Differentiation in neutral genes and a candidate gene in the pied flycatcher: using biological archives to track global climate change

Abstract

Global climate change is one of the major driving forces for adaptive shifts in migration and breeding phenology and possibly impacts demographic changes if a species fails to adapt sufficiently. In Western Europe, pied flycatchers (Ficedula hypoleuca) have insufficiently adapted their breeding phenology to the ongoing advance of food peaks within their breeding area and consequently suffered local population declines. We address the question whether this population decline led to a loss of genetic variation, using two neutral marker sets (mitochondrial control region and microsatellites), and one potentially selectively non-neutral marker (avian Clock gene). We report temporal changes in genetic diversity in extant populations and biological archives over more than a century, using samples from sites differing in the extent of climate change. Comparing genetic differentiation over this period revealed that only the recent Dutch population, which underwent population declines, showed slightly lower genetic variation than the historic Dutch population. As that loss of variation was only moderate and not observed in all markers, current gene flow across Western and Central European populations might have compensated local loss of variation over the last decades. A comparison of genetic differentiation in neutral loci versus the Clock gene locus provided evidence for stabilizing selection. Furthermore, in all genetic markers, we found a greater genetic differentiation in space than in time. This pattern suggests that local adaptation or historic processes might have a stronger effect on the population structure and genetic variation in the pied flycatcher than recent global climate changes.

Polymorphism at the Clock gene predicts phenology of long‐distance migration in birds

“…; Kuhn et al . ), this suggests no interference of latitudinal variation on the results. To sum up, poor geographical structuring of bird populations at Clock , the evidence that Clock allele length is not positively associated with wing length and the fact that genotype–phenotype associations persisted when controlling for wing length suggest that the present findings are not the spurious results of the confounding effect of latitude of origin/destination.…”

“…The heterozygosity observed in the present study (0.478) is intermediate to those reported previously (0.412–0.563; Kuhn et al . ), suggesting that at least the pied flycatcher population(s) we sampled is representative of genetic variation at Clock at continental scale.…”

The use of museum specimens with high-throughput DNA sequencers

“…Historical samples also enable direct assessment of changes in the genetics of populations over time. Such time series studies have been able to document selective sweeps of alleles associated with insecticide or herbicide resistance after introduction of chemicals (Hartley et al, 2006; Délye et al, 2013), or changes over time in genetic variation within populations in response to recent climate change (Rubidge et al, 2012; Bi et al, 2013; Kuhn et al, 2013). They also allow measures of evolutionary processes such as lineage sorting (Mende and Hundsdoerfer, 2013), and even the effects of pathogens on populations, such as the extinction of the Christmas Island rat after the introduction of a trypanosome parasite (Wyatt et al, 2008).…”

Circadian genes polymorphism and breeding phenology in a resident bird, the yellow‐legged gull

“…These findings are in line with an increasing body of evidence showing that differences in polymorphism in photoperiodic genes, especially Clock r1 and Adcyap1 , often occur among geographically distinct populations (Johnsen et al ., ; O'Malley & Banks, ; O'Malley et al ., ; Kuhn et al ., ; Bazzi et al ., ). Comparisons of latitudinal clines in allele frequency and in the gene‐phenotype associations depending on the breeding latitude in the yellow‐legged gull would help to establish whether variation at these genes may have played a role in adaptation to local environments, like in other vertebrates (Johnsen et al ., ; O'Malley & Banks, ; O'Malley et al ., ).…”

“…Within‐population polymorphism at the Clock poly‐Q region has been observed to predict the schedule of crucial annual events, such as reproduction, incubation, moult and migration (Liedvogel et al ., ; Caprioli et al ., ; Saino et al ., , ; Bazzi et al ., ), with individuals bearing more glutamine residues showing a delayed phenology compared to those which possess ‘shorter’ alleles. However, other studies have failed to find any significant association between Clock allele size and timing of phenophases (Liedvogel & Sheldon, ; Dor et al ., ; Chakarov et al ., ; Kuhn et al ., ; Peterson et al ., ).…”