Bernard J. Crespi

The evolution of social behavior in microorganisms

Recent studies of microorganisms have revealed diverse complex social behaviors, including cooperation in foraging, building, reproducing, dispersing and communicating. These microorganisms should provide novel, tractable systems for the analysis of social evolution. The application of evolutionary and ecological theory to understanding their behavior will aid in developing better means to control the many pathogenic bacteria that use social interactions to affect humans.

Host-plant adaptation drives the parallel evolution of reproductive isolation

Parallel evolution of similar traits in independent populations that inhabit ecologically similar environments strongly implicates natural selection as the cause of evolution. Parallel speciation is a special form of parallel evolution where traits that determine reproductive isolation evolve repeatedly, in closely related populations, as by-products of adaptation to ecological conditions. The outcome of such parallel evolution is that ecologically divergent pairs of populations exhibit greater levels of reproductive isolation than ecologically similar pairs of populations of a similar or younger age. The parallel evolution of reproductive isolation provides strong evidence for natural selection in the process of speciation, but only one conclusive example from nature is known. Populations of the walking-stick insect Timema cristinae that use different host-plant species have diverged in body size and shape, host preference, behaviour and the relative frequency of two highly cryptic colour-pattern morphs. Here we report that divergent selection for host adaptation, and not genetic drift, has promoted the parallel evolution of sexual isolation in this species. Our findings represent a clear demonstration that host-plant adaptation can play a crucial and repeatable role in the early stages of speciation.

Psychosis and autism as diametrical disorders of the social brain

Autistic-spectrum conditions and psychotic-spectrum conditions (mainly schizophrenia, bipolar disorder, and major depression) represent two major suites of disorders of human cognition, affect, and behavior that involve altered development and function of the social brain. We describe evidence that a large set of phenotypic traits exhibit diametrically opposite phenotypes in autistic-spectrum versus psychotic-spectrum conditions, with a focus on schizophrenia. This suite of traits is inter-correlated, in that autism involves a general pattern of constrained overgrowth, whereas schizophrenia involves undergrowth. These disorders also exhibit diametric patterns for traits related to social brain development, including aspects of gaze, agency, social cognition, local versus global processing, language, and behavior. Social cognition is thus underdeveloped in autistic-spectrum conditions and hyper-developed on the psychotic spectrum.;>We propose and evaluate a novel hypothesis that may help to explain these diametric phenotypes: that the development of these two sets of conditions is mediated in part by alterations of genomic imprinting. Evidence regarding the genetic, physiological, neurological, and psychological underpinnings of psychotic-spectrum conditions supports the hypothesis that the etiologies of these conditions involve biases towards increased relative effects from imprinted genes with maternal expression, which engender a general pattern of undergrowth. By contrast, autistic-spectrum conditions appear to involve increased relative bias towards effects of paternally expressed genes, which mediate overgrowth. This hypothesis provides a simple yet comprehensive theory, grounded in evolutionary biology and genetics, for understanding the causes and phenotypes of autistic-spectrum and psychotic-spectrum conditions.

Causes of assortative mating in arthropods

Abstract Assortative mating by size, one of the most common mating patterns in natural populations, may be explained by three hypotheses: (1) mate choice, whereby large males, large females or large individuals of both sexes choose large mates because they benefit reproductively and are differentially capable of exercising choice; (2) mate availability, whereby large females or large individuals of both sexes are differentially available for mating because of size-differential variation in mating probability or timing that is unrelated to mate choice; and (3) mating constraints, whereby relative size differences between males and females cause physical or energetic difficulties with courtship, pairing or mating. Analysis of the causes of assortative mating in well-studied arthropod species provides some support for each hypothesis in one or more species. However, comparative analysis of many species indicates that assortative mating is most closely associated with the pattern of large size of paired males and females relative to unpaired males and females and the occurrence of long pairing durations and male fighting. These comparative data therefore implicate two hypotheses for the causes of assortative mating in most arthropods: male choice of large females combined with male-male competition, and increased availability of large females combined with male-male competition. The female availability hypothesis may be more plausible because male choice and male-male competition are apparently antagonistic processes whose effects usually do not coincide. Distinguishing between hypotheses based on mate choice, mate availability and mating constraints is crucial to understanding the roles of natural selection and sexual selection in causing assortative mating.

Stick insect genomes reveal natural selection's role in parallel speciation.

Stick to the Bush Can the underlying genetic changes driving the divergence of populations into new species be predicted or repeated? Soria-Carrasco et al. (p. 738) investigated the genetic changes observed after one generation when stick insect (Timema cristinae) populations were transplanted from their preferred host plants to alternative hosts. Diverged genetic regions were relatively small, with most loci showing divergence in a single population pair. However, the number of loci showing parallel divergence was greater than expected by chance. Thus, selection can drive parallel phenotypic evolution via parallel genetic changes. Parallel speciation in insects shows both convergent and divergent selection after one generation. Natural selection can drive the repeated evolution of reproductive isolation, but the genomic basis of parallel speciation remains poorly understood. We analyzed whole-genome divergence between replicate pairs of stick insect populations that are adapted to different host plants and undergoing parallel speciation. We found thousands of modest-sized genomic regions of accentuated divergence between populations, most of which are unique to individual population pairs. We also detected parallel genomic divergence across population pairs involving an excess of coding genes with specific molecular functions. Regions of parallel genomic divergence in nature exhibited exceptional allele frequency changes between hosts in a field transplant experiment. The results advance understanding of biological diversification by providing convergent observational and experimental evidence for selection’s role in driving repeatable genomic divergence.

Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement

Recent years have seen a resurgence of interest in the process of speciation but few studies have elucidated the mechanisms either driving or constraining the evolution of reproductive isolation. In theory, the direct effects of reinforcing selection for increased mating discrimination where interbreeding produces hybrid offspring with low fitness and the indirect effects of adaptation to different environments can both promote speciation. Conversely, high levels of homogenizing gene flow can counteract the forces of selection. We demonstrate the opposing effects of reinforcing selection and gene flow in Timema cristinae walking-stick insects. The magnitude of female mating discrimination against males from other populations is greatest when migration rates between populations adapted to alternate host plants are high enough to allow the evolution of reinforcement, but low enough to prevent gene flow from eroding adaptive divergence in mate choice. Moreover, reproductive isolation is strongest under the combined effects of reinforcement and adaptation to alternate host plants. Our findings demonstrate the joint effects of reinforcement, ecological adaptation and gene flow on progress towards speciation in the wild.

Parent‐Offspring Conflict in the Evolution of Vertebrate Reproductive Mode

We propose and evaluate the hypothesis that parent‐offspring conflict over the degree of maternal investment has been one of the main selective factors in the evolution of vertebrate reproductive mode. This hypothesis is supported by data showing that the assumptions of parent‐offspring conflict theory are met for relevant taxa; the high number of independent origins of viviparity, matrotrophy (direct maternal‐fetal nutrient transfer), and hemochorial placentation (direct fetal access to the maternal bloodstream); the extreme diversity in physiological and morphological aspects of viviparity and placentation, which usually cannot be ascribed adaptive significance in terms of ecological factors; and divergent and convergent patterns in the diversification of placental structure, function, and developmental genetics. This hypothesis is also supported by data demonstrating that embryos and fetuses actively manipulate their interaction with the mother, thereby garnishing increased maternal resources. Our results indicate that selection may favor adaptations of the mother, the fetus, or both in traits related to reproductive mode and that integration of physiological and morphological data with evolutionary ecological data will be required to understand the adaptive significance of interspecific variation in viviparity, matrotrophy, and placentation.

Evolution in health and medicine Sackler colloquium: Comparative genomics of autism and schizophrenia.

We used data from studies of copy-number variants (CNVs), single-gene associations, growth-signaling pathways, and intermediate phenotypes associated with brain growth to evaluate four alternative hypotheses for the genomic and developmental relationships between autism and schizophrenia: (i) autism subsumed in schizophrenia, (ii) independence, (iii) diametric, and (iv) partial overlap. Data from CNVs provides statistical support for the hypothesis that autism and schizophrenia are associated with reciprocal variants, such that at four loci, deletions predispose to one disorder, whereas duplications predispose to the other. Data from single-gene studies are inconsistent with a hypothesis based on independence, in that autism and schizophrenia share associated genes more often than expected by chance. However, differentiation between the partial overlap and diametric hypotheses using these data is precluded by limited overlap in the specific genetic markers analyzed in both autism and schizophrenia. Evidence from the effects of risk variants on growth-signaling pathways shows that autism-spectrum conditions tend to be associated with up-regulation of pathways due to loss of function mutations in negative regulators, whereas schizophrenia is associated with reduced pathway activation. Finally, data from studies of head and brain size phenotypes indicate that autism is commonly associated with developmentally-enhanced brain growth, whereas schizophrenia is characterized, on average, by reduced brain growth. These convergent lines of evidence appear most compatible with the hypothesis that autism and schizophrenia represent diametric conditions with regard to their genomic underpinnings, neurodevelopmental bases, and phenotypic manifestations as reflecting under-development versus dysregulated over-development of the human social brain.

Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks

Abstract Population differentiation often reflects a balance between divergent natural selection and the opportunity for homogenizing gene flow to erode the effects of selection. However, during ecological speciation, trait divergence results in reproductive isolation and becomes a cause, rather than a consequence, of reductions in gene flow. To assess both the causes and the reproductive consequences of morphological differentiation, we examined morphological divergence and sexual isolation among 17 populations of Timema cristinae walking‐sticks. Individuals from populations adapted to using Adenostoma as a host plant tended to exhibit smaller overall body size, wide heads, and short legs relative to individuals using Ceonothus as a host. However, there was also significant variation in morphology among populations within host‐plant species. Mean trait values for each single population could be reliably predicted based upon host‐plant used and the potential for homogenizing gene flow, inferred from the size of the neighboring population using the alternate host and mitochondrial DNA estimates of gene flow. Morphology did not influence the probability of copulation in between‐population mating trials. Thus, morphological divergence is facilitated by reductions in gene flow, but does not cause reductions in gene flow via the evolution of sexual isolation. Combined with rearing data indicating that size and shape have a partial genetic basis, evidence for parallel origins of the host‐associated forms, and inferences from functional morphology, these results indicate that morphological divergence in T. cristinae reflects a balance between the effects of host‐specific natural selection and gene flow. Our findings illustrate how data on mating preferences can help determine the causal associations between trait divergence and levels of gene flow.

Comparative genomics of autism and schizophrenia

We used data from studies of copy-number variants (CNVs), single-gene associations, growth-signaling pathways, and intermediate phenotypes associated with brain growth to evaluate four alternative hypotheses for the genomic and developmental relationships between autism and schizophrenia: (i) autism subsumed in schizophrenia, (ii) independence, (iii) diametric, and (iv) partial overlap. Data from CNVs provides statistical support for the hypothesis that autism and schizophrenia are associated with reciprocal variants, such that at four loci, deletions predispose to one disorder, whereas duplications predispose to the other. Data from single-gene studies are inconsistent with a hypothesis based on independence, in that autism and schizophrenia share associated genes more often than expected by chance. However, differentiation between the partial overlap and diametric hypotheses using these data is precluded by limited overlap in the specific genetic markers analyzed in both autism and schizophrenia. Evidence from the effects of risk variants on growth-signaling pathways shows that autism-spectrum conditions tend to be associated with up-regulation of pathways due to loss of function mutations in negative regulators, whereas schizophrenia is associated with reduced pathway activation. Finally, data from studies of head and brain size phenotypes indicate that autism is commonly associated with developmentally-enhanced brain growth, whereas schizophrenia is characterized, on average, by reduced brain growth. These convergent lines of evidence appear most compatible with the hypothesis that autism and schizophrenia represent diametric conditions with regard to their genomic underpinnings, neurodevelopmental bases, and phenotypic manifestations as reflecting under-development versus dysregulated over-development of the human social brain.