Does genetic differentiation underlie behavioral divergence in response to migration barriers in sticklebacks? A common garden experiment

Water management measures in the 1970s in the Netherlands have produced a large number of “resident” populations of three-spined sticklebacks that are no longer able to migrate to the sea. This may be viewed as a replicated field experiment, allowing us to study how the resident populations are coping with human-induced barriers to migration. We have previously shown that residents are smaller, bolder, more exploratory, more active, and more aggressive and exhibited lower shoaling and lower migratory tendencies compared to their ancestral “migrant” counterparts. However, it is not clear if these differences in wild-caught residents and migrants reflect genetic differentiation, rather than different developmental conditions. To investigate this, we raised offspring of four crosses (migrant ♂ × migrant ♀, resident ♂ × resident ♀, migrant ♂ × resident ♀, resident ♂ × migrant ♀) under similar controlled conditions and tested for differences in morphology and behavior as adults. We found that lab-raised resident sticklebacks exhibited lower shoaling and migratory tendencies as compared to lab-raised migrants, retaining the differences in their wild-caught parents. This indicates genetic differentiation of these traits. For all other traits, the lab-raised sticklebacks of the various crosses did not differ significantly, suggesting that the earlier-found contrast between wild-caught fish reflects differences in their environment. Our study shows that barriers to migration can lead to rapid differentiation in behavioral tendencies over contemporary timescales (~ 50 generations) and that part of these differences reflects genetic differentiation. Significance statement Many organisms face changes to their habitats due to human activities. Much research is therefore dedicated to the question whether and how organisms are able to adapt to novel conditions. We address this question in three-spined sticklebacks, where water management measures cut off some populations, prohibiting their seasonal migration to the North Sea. In a previous study, we showed that wild-caught “resident” fish exhibited markedly different behavior than migrants. To disentangle whether these differences reflect genetic differentiation or differences in the conditions under which the wild-caught fish grew up, we conducted crosses, raising the F1 offspring under identical conditions. As their wild-caught parents, the F1 of resident × resident crosses exhibited lower migratory and shoaling tendencies than the F1 of migrant × migrant crosses, while the F1 of hybrid crosses were intermediate. This suggests that ~ 50 years of isolation are sufficient to induce behaviorally relevant genetic differentiation.

Autism Spectrum Disorders: Analysis of Mobile Elements at 7q11.23 Williams–Beuren Region by Comparative Genomics

Autism spectrum disorders (ASD) are a group of complex neurodevelopmental disorders, characterized by a deficit in social interaction and communication. Many genetic variants are associated with ASD, including duplication of 7q11.23 encompassing 26–28 genes. Symmetrically, the hemizygous deletion of 7q11.23 causes Williams–Beuren syndrome (WBS), a multisystem disorder characterized by “hyper-sociability” and communication skills. Interestingly, deletion of four non-exonic mobile elements (MEs) in the “canine WBS locus” were associated with the behavioral divergence between the wolf and the dog and dog sociability and domestication. We hypothesized that indel of these MEs could be involved in ASD, associated with its different phenotypes and useful as biomarkers for patient stratification and therapeutic design. Since these MEs are non-exonic they have never been discovered before. We searched the corresponding MEs and loci in humans by comparative genomics. Interestingly, they mapped on different but ASD related genes. The loci in individuals with phenotypically different autism and neurotypical controls were amplified by PCR. A sub-set of each amplicon was sequenced by Sanger. No variant resulted associated with ASD and neither specific phenotypes were found but novel small-scale insertions and SNPs were discovered. Since MEs are hyper-methylated and epigenetically modulate gene expression, further investigation in ASD is necessary.

Intraspecific facial bite marks in tyrannosaurids provide insight into sexual maturity and evolution of bird-like intersexual display

Intraspecific aggression, or agonism, is a widespread intrasexual selective behavior important to understanding animal behavioral ecology and reproductive systems. Such behavior can be studied either by direct observation or inferred from wound/scar frequency in extant species but is difficult to document in extinct taxa, limiting understanding of its evolution. Among extant archosaurs, crocodylians display extensive intrasexual aggression, whereas birds show extreme visual/vocal intersexual display. The evolutionary origin of this behavioral divergence, and pattern in non-avian dinosaurs, is unknown. Here we document the morphology, frequency, and ontogeny of intraspecific facial bite lesions (324 lesions) in a large sample of tyrannosaurids (202 specimens, 528 elements) to infer patterns of intraspecific aggression in non-avian theropods. Facial scars are consistent in position and orientation across tyrannosaurid species, suggesting bites were inflicted due to repeated/postured behavior. Facial scars are absent in young tyrannosaurids, first appear in immature animals (~50% adult skull length), are present in ~60% of the adult-sized specimens, and show aggressor:victim size isometry. The ontogenetic distribution of bite scars suggests agonistic behavior is associated with the onset of sexual maturity, and scar presence in approximately half the specimens may relate to a sexual pattern. Considered in a phylogenetic context, intraspecific bite marks are consistent and widely distributed in fossil and extant crocodyliforms and non-maniraptoriform theropods, suggesting a potential plesiomorphic behavior in archosaurs. Their absence in maniraptoriform theropods, including birds, may reflect a transition from boney cranial ornamentation and crocodylian-like intrasexual aggression to avian-like intersexual display with the evolution of pennaceous feathers.

Consequences of coupled barriers to gene flow for the build-up of genomic differentiation: Reproductive barriers and coupling in corn borers

ABSTRACTTheory predicts that when different barriers to gene flow become coincident, their joint effects enhance reproductive isolation and genomic divergence beyond their individual effects, but empirical tests of this ‘coupling’ hypothesis are rare. Here, we analyze patterns of gene exchange among populations of European corn borer moths that vary in the number of acting barriers, allowing for comparisons of genomic variation when barrier traits or loci are in coincident or independent states. We find that divergence is mainly restricted to barrier loci when populations differ by a single barrier, whereas the coincidence of temporal and behavioral barriers is associated with divergence of two chromosomes harboring barrier loci. Furthermore, differentiation at temporal barrier loci increases in the presence of behavioral divergence, while differentiation at behavioral barrier loci increases in the presence of temporal divergence. Our results demonstrate how the joint action of coincident barrier effects leads to levels of genomic differentiation that far exceed those of single barriers acting alone, consistent with theory arguing that coupling allows indirect selection to combine with direct selection and thereby lead to a stronger overall barrier to gene flow. Thus, the state of barriers – independent or coupled – strongly influences the accumulation of genomic differentiation.

Does genetic differentiation underlie behavioral divergence in response to migration barriers in sticklebacks? A common garden experiment

Water management measures in the 1970s in the Netherlands have produced a large number of ‘resident’ populations of three-spined sticklebacks that are no longer able to migrate to the sea. This may be viewed as a replicated field experiment, allowing us to study how the resident populations are coping with human-induced barriers to migration. We have previously shown that residents are smaller, bolder, more exploratory, more active, more aggressive, exhibited lower shoaling and lower migratory tendencies compared to their ancestral ‘migrant’ counterparts. However, it is not clear if these differences in wild-caught residents and migrants reflect genetic differentiation, rather than different developmental conditions. To investigate this, we raised offspring of four crosses (migrant ♂ x migrant ♀, resident ♂ x resident ♀, migrant ♂ x resident ♀, resident ♂ x migrant ♀) under similar controlled conditions and tested for differences in morphology and behavior as adults. We found that lab-raised resident sticklebacks exhibited lower shoaling and migratory tendencies as compared to lab-raised migrants, retaining the differences in their wild-caught parents. This indicates genetic differentiation of these traits. For all other traits, the lab-raised sticklebacks of the various crosses did not differ significantly, suggesting that the earlier-found contrast between wild-caught fish reflect differences in their environment. Our study shows that barriers to migration can lead to rapid differentiation in behavioral tendencies over contemporary timescales (∼50 generations), and that part of these differences reflects genetic differentiation.Significance statementMany organisms face changes to their habitats due to human activities. Much research is therefore dedicated to the question whether and how organisms are able to adapt to novel conditions. We address this question in three-spined sticklebacks, where water management measures cut off some populations, prohibiting their seasonal migration to the North Sea. In a previous study, we showed that wild-caught ‘resident’ fish exhibited markedly different behavior than migrants. To disentangle whether these differences reflect genetic differentiation or differences in the conditions under which the wild-caught fish grew up, we conducted crosses, raising the F1 offspring under identical conditions. As their wild-caught parents, the F1 of resident x resident crosses exhibited lower migratory and shoaling tendencies than the F1 of migrant x migrant crosses, while the F1 of hybrid crosses were intermediate. This suggests that ∼50 years of isolation are sufficient to induce behaviorally relevant genetic differentiation.

Habitat fragmentation induces rapid divergence of migratory and isolated sticklebacks

The adaptive capacity of many organisms is seriously challenged by human-imposed environmental change, which currently happens at unprecedented rates and magnitudes. For migratory fish, habitat fragmentation is a major challenge that can compromise their survival and reproduction. Therefore, it is important to study if fish populations can adapt to such modifications of their habitat. Here, we study whether originally anadromous three-spined stickleback populations (Gasterosteus aculeatus; "migrants") changed in behavior and morphology in response to human-induced isolation. We made use of a natural field-experiment, where the construction of pumping stations and sluices in the 1970s unintendedly created replicates of land-locked stickleback populations ("resident") in the Netherlands. For two years, we systematically tested populations of residents and migrants for differences in morphology and behavioral traits (activity, aggressiveness, exploration, boldness and shoaling) in lab-based assays. We detected differences between migrant and resident populations in virtually all phenotypic traits studied: compared to the ancestral migrants, residents were smaller in size, had fewer and smaller plates and were significantly more active, aggressive, exploratory and bolder and shoaled less. Despite large ecological differences between 2018 and 2019, results were largely consistent across the two years. Our study shows that human-induced environmental change has led to the rapid and consistent morphological and behavioral divergence of stickleback populations in about 50 generations. Such changes may be adaptive but this remains to be tested.

Larval breeding sites of the mosquito Aedes aegypti in forest and domestic habitats in Africa and the potential association with oviposition evolution

Adaptations to anthropogenic domestic habitats contribute to the success of mosquito Aedes aegypti as a major global vector of several arboviral diseases. The species inhabited African forests before expanding into domestic habitats and spreading to the rest of the world. Despite a well-studied evolutionary history, how this species initially moved into human settlements in Africa remains unclear. During this initial habitat transition, Ae. aegypti switched from using natural containers like tree holes as larval breeding sites to using artificial containers like clay pots. Little is known about how these natural versus artificial containers differ in their environments, or whether Ae. aegypti in forest versus domestic habitats evolved any corresponding incipient behavioral divergence, such as in oviposition. To address these gaps, we first characterized physical characteristics, larval density, microbial density, bacterial composition, and volatile profiles of natural versus artificial containers used as mosquito larval breeding sites. We focused on two localities in Africa, La Lopé, Gabon and Rabai, Kenya. In both localities, our data showed that the two habitat-specific container types had significantly different characteristics. We then examined whether such containers differed in their attractiveness for oviposition, a key behavior affecting larval distribution. Forest Ae. aegypti readily accepted artificial containers in our field experiments, and laboratory choice experiments did not find distinct oviposition preference between forest and village Ae. aegypti colonies. These results suggested that African Ae. aegypti were likely generalists in their oviposition site choice. This flexibility to accept different containers might play a vital role during the initial domestication of Ae. aegypti, allowing the mosquitoes to use human-stored water as fallback breeding sites during dry seasons. Although ovipositional changes were not present initially, after longer domestic habitat breeding, the mosquitoes did evolve divergence oviposition preference, as suggested by previous comparisons of African Ae. aegypti and human-specialized non-African Ae. aegypti.

Second-wave Dynamics of COVID-19: Impact of Behavioral Changes, Immunity Loss, New Strains, and Vaccination

An epidemiological model for COVID-19 developed earlier was extended to determine the effects of behavioral changes, immunity loss, and vaccination on second and subsequent wave dynamics of the pandemic. A model variant that distinguishes four demographic groups with different infection rates and mortality rates was developed to test the hypothesis that behavioral divergence between groups can explain both the larger incidence and lower mortality rate of COVID-19’s second wave. A model version that incorporates immunity loss was developed to test the hypothesis that immunity loss can explain the second wave. Simulations indicate that of the two hypotheses, only the former is consistent with observed trends. Nevertheless, loss of immunity can significantly increase total number of deaths in the long run, particularly in cases where vaccine distribution is barely sufficient to reach herd immunity. The observed trends are illustrated with detailed simulations of the progression of COVID-19 in the United Kingdom, including the appearance of new strains. The U.K. case study indicates the extent to which NPI can be relaxed during the distribution of the vaccine.

Contribution of TRESK two-pore domain potassium channel to bone cancer-induced spontaneous pain and evoked cutaneous pain in rats

Cancer-associated pain is debilitating. However, the mechanism underlying cancer-induced spontaneous pain and evoked pain remains unclear. Here, using behavioral tests with immunofluorescent staining, overexpression, and knockdown of TRESK methods, we found an extensive distribution of TRESK potassium channel on both CGRP+ and IB4+ nerve fibers in the hindpaw skin, on CGRP+ nerve fibers in the tibial periosteum which lacks IB4+ fibers innervation, and on CGRP+ and IB4+ dorsal root ganglion (DRG) neurons in rats. Moreover, we found a decreased expression of TRESK in the corresponding nerve fibers within the hindpaw skin, the tibial periosteum and the DRG neurons in bone cancer rats. Overexpression of TRESK in DRG neurons attenuated both cancer-induced spontaneous pain (partly reflect skeletal pain) and evoked pain (reflect cutaneous pain) in tumor-bearing rats, in which the relief of evoked pain is time delayed than spontaneous pain. In contrast, knockdown of TRESK in DRG neurons produced both spontaneous pain and evoked pain in naïve rats. These results suggested that the differential distribution and decreased expression of TRESK in the periosteum and skin, which is attributed to the lack of IB4+ fibers innervation within the periosteum of the tibia, probably contribute to the behavioral divergence of cancer-induced spontaneous pain and evoked pain in bone cancer rats. Thus, the assessment of spontaneous pain and evoked pain should be accomplished simultaneously when evaluating the effect of some novel analgesics in animal models. Also, this study provides solid evidence for the role of peripheral TRESK in both cancer-induced spontaneous pain and evoked cutaneous pain.