Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation.

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as 'Isolation by Adaptation' (IBA). IBA can be complementary to the well-known pattern of 'Isolation by Distance' (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome-wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole genome sequence for H. rustica, to which we aligned a set of 9,493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behavior and sexual signaling, as well as geographic distance together, explain over 70% of genome-wide divergence among populations. Controlling for IBD, we find 42% of genome-wide divergence is attributable to IBA through pairwise differences in traits related to migratory behavior and sexual signaling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population-level differentiation in this group of closely related populations. This article is protected by copyright. All rights reserved

Low Variation in the Polymorphic Clock Gene Poly-Q Region Despite Population Genetic Structure across Barn Swallow (Hirundo rustica) Populations

Recent studies of several species have reported a latitudinal cline in the circadian clock gene, Clock, which influences rhythms in both physiology and behavior. Latitudinal variation in this gene may hence reflect local adaptation to seasonal variation. In some bird populations, there is also an among-individual association between Clock poly-Q genotype and clutch initiation date and incubation period. We examined Clock poly-Q allele variation in the Barn Swallow (Hirundo rustica), a species with a cosmopolitan geographic distribution and considerable variation in life-history traits that may be influenced by the circadian clock. We genotyped Barn Swallows from five populations (from three subspecies) and compared variation at the Clock locus to that at microsatellite loci and mitochondrial DNA (mtDNA). We found very low variation in the Clock poly-Q region, as >96% of individuals were homozygous, and the two other alleles at this locus were globally rare. Genetic differentiation based on the Clock poly-Q locus was not correlated with genetic differentiation based on either microsatellite loci or mtDNA sequences. Our results show that high diversity in Clock poly-Q is not general across avian species. The low Clock variation in the background of heterogeneity in microsatellite and mtDNA loci in Barn Swallows may be an outcome of stabilizing selection on the Clock locus

The symbiotic magnetic-sensing hypothesis: do Magnetotactic Bacteria underlie the magnetic sensing capability of animals?

Abstract The ability to sense Earth’s magnetic field has evolved in various taxa. However, despite great efforts to find the ‘magnetic-sensor’ in vertebrates, the results of these scientific efforts remain inconclusive. A few decades ago, it was found that bacteria, known as magnetotactic bacteria (MTB), can move along a magnetic field using nanometric chain-like structures. Still, it is not fully clear why these bacteria evolved to have this capacity. Thus, while for MTB the ‘magnetic-sensor’ is known but the adaptive value is still under debate, for metazoa it is the other way around. In the absence of convincing evidence for any ‘magnetic-sensor’ in metazoan species sensitive to Earth’s magnetic field, we hypothesize that a mutualism between these species and MTB provides one. In this relationship the host benefits from a magnetotactic capacity, while the bacteria benefit a hosting environment and dispersal. We provide support for this hypothesis using existing literature, demonstrating that by placing the MTB as the ‘magnetic-sensor’, previously contradictory results are now in agreement. We also propose plausible mechanisms and ways to test the hypothesis. If proven correct, this hypothesis would shed light on the forces driving both animal and bacteria magnetotactic abilities

Data from: Cortisol advantage of neighbouring the opposite sex in utero

Population sex ratios naturally fluctuate around equality. It is argued that the production of an equal number of male and female offspring by individual parents should be favoured by selection, if all costs and benefits are equal. Theoretically, an even-sex ratio should yield the highest probability for a fetus to be adjacent to a fetus of the opposite sex in utero. This may cause developmental costs or benefits that have been overlooked. We examined the physiological and developmental parameters associated with in utero sex ratios in the nutria (Myocastor coypus), an invasive wildlife species with a strong reproductive output. Using hair-testing, we found that litters with even-sex ratios had the highest average cortisol levels. Fetuses neighbouring the opposite sex exhibited longer trunks than those neighbouring the same sex, which might imply better lung development. Our results are the first to link intra-utero sex ratios and fetal cortisol and suggest that fetal cortisol might be a mechanism by which even-sex ratios are maintained via developmental advantages

pups averages 2013-2015

Data for litters, including averages

individual fetuses 2013-2015

Data for individual fetuses

Data from: Multiple sexual signals and behavioral reproductive isolation in a diverging population

Sexual trait divergence has been shown to play a role in the evolution of reproductive isolation. While variation in multiple sexual signals is common among closely related species, little is known about the role of these different axes of phenotype variation with respect to the evolution of behavioral reproductive isolation. Here we study a unique population of barn swallows (Hirundo rustica transitiva) which can only be distinguished phenotypically from its neighboring populations based on two features of male plumage: exaggerated expression of both long tail streamers and dark ventral coloration. Using phenotype manipulation experiments, we conducted a paternity study to examine whether both traits are sexually selected. Our results show that an exaggerated form of the local male phenotype (with both tail elongation and color darkening) is favored by local females whereas males whose phenotypes were manipulated to look like males of neighboring subspecies suffered paternity losses from their social mates. These results confirm the multiple signaling role of the unique tail and color combination in our diverging population and suggest a novel possibility according to which multiple sexual signals may also be used to discriminate among males from nearby populations when pre-zygotic reproductive isolation is adaptive

The maintenance of phenotypic divergence through sexual selection: An experimental study in barn swallows \u3ci\u3eHirundo rustica\u3c/i\u3e

Previous studies have shown that sexual signals can rapidly diverge among closely related species. However, we lack experimental studies to demonstrate that differences in trait-associated reproductive performance maintain sexual trait differences between closely related populations, in support for a role of sexual selection in speciation. Populations of Northern Hemisphere distributed barn swallows Hirundo rustica are closely related, yet differ in two plumage-based traits: ventral color and length of the outermost tail feathers (streamers). Here we provide experimental evidence that manipulations of these traits result in different reproductive consequences in two subspecies of barn swallow: (H. r. erythrogaster in North America and H. r. transitiva in the East Mediterranean). Experimental results in Colorado, USA, demonstrate that males with (1) darkened ventral coloration and (2) shortened streamers gained paternity between two successive reproductive bouts. In contrast, exaggeration of both traits improved reproductive performance within H. r. transitiva in Israel: males with a combination treatment of darkened ventral coloration and elongated streamers gained paternity between two successive reproductive bouts. Collectively, these experimental results fill an important gap in our understanding for how divergent sexual selection maintains phenotype differentiation in closely related populations, an important aspect of the speciation process. Includes supplementary materials

Data from: Expression of multiple sexual signals by fathers and sons in the East-Mediterranean barn swallow: Are advertising strategies heritable?

The level of expression of sexually selected traits is generally determined by genes, environment and their interaction. In species that use multiple sexual signals which may be costly to produce, investing in the expression of one sexual signal may limit the expression of the other, favoring the evolution of a strategy for resource allocation among signals. As a result, even when the expression of sexual signals is condition dependent, the relative level of expression of each signal may be heritable. We tested this hypothesis in the East-Mediterranean barn swallow (Hirundo rustica transitiva), in which males have been shown to express two uncorrelated sexual signals: red-brown ventral coloration, and long tail streamers. We show that variation in both signals may partially be explained by age, as well as by paternal origin (genetic father-son regressions), but that the strongest similarity between fathers and sons is the relative allocation towards one trait or the other (relative expression index), rather than the expression of the traits themselves. These results suggest that the expression of one signal is not independent of the other, and that genetic strategies for resource allocation among sexual signals may be selected for during the evolution of multiple sexual signals

Expression of multiple sexual signals by fathers and sons in the East-Mediterranean barn swallow: are advertising strategies heritable?

The level of expression of sexually selected traits is generally determined by genes, environment and their interaction. In species that use multiple sexual signals which may be costly to produce, investing in the expression of one sexual signal may limit the expression of the other, favoring the evolution of a strategy for resource allocation among signals. As a result, even when the expression of sexual signals is condition dependent, the relative level of expression of each signal may be heritable. We tested this hypothesis in the East-Mediterranean barn swallow (Hirundo rustica transitiva), in which males have been shown to express two uncorrelated sexual signals: red-brown ventral coloration, and long tail streamers. We show that variation in both signals may partially be explained by age, as well as by paternal origin (genetic father-son regressions), but that the strongest similarity between fathers and sons is the relative allocation towards one trait or the other (relative expression index), rather than the expression of the traits themselves. These results suggest that the expression of one signal is not independent of the other, and that genetic strategies for resource allocation among sexual signals may be selected for during the evolution of multiple sexual signals