Biology subjects

Hoekstra, H. E.

Publications and source records attributed to Hoekstra, H. E..

9 recordsLinked to original sources

bioRxiv2018

The genetics of morphological and behavioral island traits in deer mice

Animals on islands often exhibit dramatic differences in morphology and behaviour compared to mainland individuals, a phenomenon known as the \"island syndrome\". These differences are thought to be adaptations to island environments, but the extent to which they have a genetic basis or instead represent plastic responses to environmental extremes is often unknown. Here, we revisit a classic case of island syndrome in deer mice (Peromyscus maniculatus) from British Columbia. We first show that Saturna Island mice and those from neighbouring islands are [~]35% ([~]5g) heavier than mainland mice and diverged approximately 10 thousand years ago. We then established laboratory colonies and find that Saturna Island mice are heavier both because they are longer and have disproportionately more lean mass. These trait differences are maintained in second-generation captive-born mice raised in a common environment. In addition, island-mainland hybrids reveal a maternal genetic effect on body weight. Using behavioural testing in the lab, we also find that wild-caught island mice are less aggressive than mainland mice; however, lab-raised mice born to these founders do not differ in aggression. Together, our results reveal that these mice respond differently to environmental conditions on islands - evolving both heritable changes in a morphological trait and also expressing a plastic phenotypic response in a behavioural trait.

evolutionary biology↗

bioRxiv2018

The fitness consequences of genetic variation in wild populations of mice

Adaptive evolution can occur when genetic change affects traits subject to natural selection. Although selection is a deterministic process, adaptation can be difficult to predict in finite populations because the functional connections between genotype, phenotype, and fitness are complex. Here, we make these connections using a combination of field and laboratory experiments. We conduct a large-scale manipulative field experiment with wild populations of deer mice in distinct habitats to directly estimate natural selection on pigmentation traits and next test whether this selection drives changes in allele frequency at an underlying pigment locus. We find that divergent cryptic phenotypes are repeatedly favoured in each habitat, leaving footprints of selection in the Agouti gene. Next, using transgenic experiments in Mus, we functionally test one of the Agouti mutations associated with survival, a Serine deletion in exon 2, and find that it causes lighter coat colour via changes in its protein binding properties. Finally, we show significant change in the frequency of this mutation in our field experiment. Together, our findings demonstrate how a sequence variant alters phenotype and show the ensuing ecological consequences that drive changes in population allele frequency, thereby revealing the full process of evolution by natural selection.

evolutionary biology↗

bioRxiv2018

Diet-based assortative mating through sexual imprinting

Speciation is facilitated when traits subject to divergent selection also contribute to non-random mating--so-called magic traits. Diet is a potential magic trait in animal populations because selection for divergence in consumed food may contribute to assortative mating and therefore sexual isolation. However, the mechanisms causing positive diet-based assortment are largely unknown. Here, using diet manipulations in a sexually imprinting species of mouse, Peromyscus gossypinus (the cotton mouse), we tested the hypothesis that sexual imprinting on a divergent diet could be a mechanism that generates rapid and significant sexual isolation. We provided breeding pairs with novel garlic- or orange-flavored water and assessed whether their offspring, exposed to these flavors in utero and in the nest before weaning, later preferred mates that consumed the same flavored water as their parents. While males showed no preference, females preferred males of their parental diet, which generated significant sexual isolation. Thus, our experiment demonstrates that sexual imprinting on dietary cues learned in utero and/or postnatally can facilitate reproductive isolation and potentially speciation.

evolutionary biology↗

bioRxiv2018

Sibling rivalry: Males with more brothers develop larger testes

When females mate with multiple partners in a reproductive cycle, the relative number of competing sperm from rival males is often the most critical factor in determining paternity. Gamete production is directly related to testis size in most species, and is associated with both mating behavior within a system and perceived risk of competition. Peromyscus maniculatus is naturally promiscuous and males invest significantly more in sperm production than males of P. polionotus, their monogamous sister-species. Here we show that the relatively larger testes in P. maniculatus are retained, even after decades of enforced monogamy in captivity. While these results suggest that differences in sperm production between species with divergent evolutionary histories can be maintained, we also show that the early rearing environment of males can strongly influence their testis size as adults. Using a second-generation hybrid population to increase variation in testis size, we show that males reared in litters with more brothers develop larger testes as adults. Importantly, this difference in testis size is also associated with increased fertility. Together, our findings suggest that sperm production may be both broadly shaped by natural selection over evolutionary timescales and also finely tuned during early development.

evolutionary biology↗

bioRxiv2018

Divergent genetic mechanisms lead to spiny hair in mammals

Spines, or modified hairs, have evolved multiple times in mammals, particularly in rodents. In this study, we investigated the evolution of spines in six rodent families. We first measured and compared the morphology and physical properties of hairs between paired spiny and non-spiny sister lineages. We found two distinct hair morphologies had repeatedly evolved in spiny rodents: hairs with a grooved cross-section and a second near cylindrical form. Compared to the ancestral elliptical-shaped hairs, spiny hairs had higher tension and stiffness, and overall, hairs with similar morphology had similar functional properties. To examine the genetic basis of this convergent evolution, we tested whether a single amino acid change (V370A) in the Ecdysoplasin A receptor (Edar) gene is associated with spiny hair, as this substitution causes thicker and straighter hair in East Asian human populations. We found that most mammals have the common amino acid valine at position 370, but two species, the kangaroo rat (non-spiny) and spiny pocket mouse (spiny), have an isoleucine. Importantly, none of the variants we identified are associated with differences in rodent hair morphology. Thus, the specific Edar mutation associated with variation in human hair does not seem to play a role in modifying hairs in wild rodents, suggesting that different mutations in Edar and/or other genes are responsible for variation in the spiny hair phenotypes we observed within rodents.

genetics↗

bioRxiv2017

The evolution of thermoregulatory nesting behaviour in Peromyscus mice

Structures built by animals, such as nests, often can be considered extended phenotypes that facilitate the study of animal behaviour. For rodents, nest building is both an important form of behavioural thermoregulation and a critical component of parental care. Changes in nest structure or the prioritization of nesting behaviour are therefore likely to have consequences for survival and reproduction, and both biotic and abiotic environmental factors are likely to influence the adaptive value of such differences. Here we first develop a novel assay to investigate interspecific variation in the nesting behaviour of deer mice (genus Peromyscus). Using this assay, we find that, while there is some variation in the complexity of the nests built by Peromyscus mice, differences in the latency to begin nest construction are more striking. Four of the seven taxa examined here build nests within an hour of being given nesting material, but this latency to nest is not related to ultimate differences in nest structure, suggesting that the ability to nest is relatively conserved within the genus, but species differ in their prioritization of nesting behaviour. We also find that latency to nest is not correlated with body size, climate, or the construction of burrows that create microclimates. However, the four taxa with short nesting latencies all have monogamous mating systems, suggesting that differences in nesting latency may be related to social environment. This detailed characterization of nesting behaviour within the genus provides an important foundation for future studies of the genetic and neurobiological mechanisms that contribute to the evolution of behaviour.

animal behavior and cognition↗

bioRxiv2017

The evolutionary history of Nebraska deer mice: local adaptation in the face of strong gene flow

The interplay of gene flow, genetic drift, and local selective pressure is a dynamic process that has been well studied from a theoretical perspective over the last century. Wright and Haldane laid the foundation for expectations under an island-continent model, demonstrating that an island-specific beneficial allele may be maintained locally if the selection coefficient is larger than the rate of migration of the ancestral allele from the continent. Subsequent extensions of this model have provided considerably more insight. Yet, connecting theoretical results with empirical data has proven challenging, owing to a lack of information on the relationship between genotype, phenotype, and fitness. Here, we examine the demographic and selective history of deer mice in and around the Nebraska Sand Hills, a system in which variation at the Agouti locus affects cryptic coloration that in turn affects the survival of mice in their local habitat. We first genotyped 250 individuals from eleven sites along a transect spanning the Sand Hills at 660,000 SNPs across the genome. Using these genomic data, we found that deer mice first colonized the Sand Hills following the last glacial period. Subsequent high rates of gene flow have served to homogenize the majority of the genome between populations on and off the Sand Hills, with the exception of the Agouti pigmentation locus. Furthermore, mutations at this locus are strongly associated with the pigment traits that are strongly correlated with local soil coloration and thus responsible for cryptic coloration.

evolutionary biology↗

bioRxiv2017

Evolution and genetics of precocious burrowing behavior in Peromyscus mice

A central challenge in biology is to understand how innate behaviors evolve between closely related species. One way to elucidate how differences arise is to compare the development of behavior in species with distinct adult traits. Here, we report that Peromyscus polionotus is strikingly precocious with regard to burrowing behavior, but not other behaviors, compared to its sister species P. maniculatus. In P. polionotus, burrows were excavated as early as 17 days of age, while P. maniculatus did not build burrows until 10 days later. Moreover, the well-known differences in burrow architecture between adults of these species--P. polionotus adults excavate long burrows with an escape tunnel, while P. maniculatus dig short, single-tunnel burrows--were intact in juvenile burrowers. To test whether this juvenile behavior is influenced by early-life environment, pups of both species were reciprocally cross-fostered. Fostering did not alter the characteristic burrowing behavior of either species, suggesting these differences are genetic. In backcross F2 hybrids, we show that precocious burrowing and adult tunnel length are genetically correlated, and that a single P. polionotus allele in a genomic region linked to adult tunnel length is predictive of precocious burrow construction. The co-inheritance of developmental and adult traits indicates the same genetic region--either a single gene with pleiotropic effects, or closely linked genes-- acts on distinct aspects of the same behavior across life stages. Such genetic variants likely affect behavioral drive (i.e. motivation) to burrow, and thereby affect both the development and adult expression of burrowing behavior.\n\nHighlightsO_LIJuvenile P. polionotus construct burrows precociously compared to its sister species P. maniculatus\nC_LIO_LICross-fostering does not alter species-specific burrowing behavior\nC_LIO_LIA QTL linked to adult tunnel length predicts developmental onset of burrow construction in hybrids\nC_LIO_LIPleiotropic genetic variant(s) may affect behavioral drive across life stages\nC_LI

animal behavior and cognition↗

bioRxiv2017

Sexual Imprinting And Speciation In Two Peromyscus Species

Sexual isolation, a reproductive barrier, can prevent interbreeding between diverging populations or species. Sexual isolation can have a clear genetic basis; however, it may also result from learned mate preferences that form via sexual imprinting. Here, we demonstrate that two sympatric species of mice--the white-footed mouse (Peromyscus leucopus) and its sister species, the cotton mouse (P. gossypinus)--hybridize only rarely in the wild despite co-occurrence in the same habitat and lack of any measurable intrinsic postzygotic barriers in laboratory crosses. We present evidence that strong conspecific mating preferences in each species result in significant sexual isolation. We find that these preferences are learned in at least one species: P. gossypinus sexually imprints on its parents, but in P. leucopus, additional factors influence mating preferences. Our study demonstrates that sexual imprinting contributes to reproductive isolation that reduces hybridization between otherwise interfertile species, supporting the role for learning in mammalian speciation.

evolutionary biology↗