Survival fluctuation is linked to precipitation variation during staging in a migratory shorebird.

Understanding how weather conditions affect animal populations is essential to foresee population changes in times of global climate shifts. However, assessing year-round weather impacts on demographic parameters is hampered in migratory animals due to often unknown occurrence in space and time. We addressed this by coupling tracking and weather data to explain extensive variation in apparent survival across 19 years in a northern European population of little ringed plovers (Charadrius dubius). Over 90% (n = 21) of tracked individuals followed migration routes along the Indo-European flyway to south India. Building on capture-recapture histories of nearly 1400 individuals, we found that between-year variation in precipitation during post-breeding staging in northern South Asia explained 47% of variation in apparent adult survival. Overall, the intensity of the monsoon in South Asia explained 31-33% of variability in apparent survival. In contrast, weather conditions in breeding, final non-breeding and pre-breeding quarters appeared less important in this species. The integration of multi-source data seems essential for identifying key regions and periods limiting population growth, for forecasting future changes and targeting conservation efforts.

Genetic differentiation in an endangered and strongly philopatric, migrant shorebird.

BACKGROUND: Populations living in fragmented habitats may suffer from loss of genetic variation and reduced between-patch dispersal, which are processes that can result in genetic differentiation. This occurs frequently in species with reduced mobility, whereas genetic differentiation is less common among mobile species such as migratory birds. The high dispersal capacity in the latter species usually allows for gene flow even in fragmented landscapes. However, strongly philopatric behaviour can reinforce relative isolation and the degree of genetic differentiation. The Southern Dunlin (Calidris alpina schinzii) is a philopatric, long-distance migratory shorebird and shows reduced dispersal between isolated breeding patches. The endangered population of the Southern Dunlin breeding at the Baltic Sea has suffered from habitat deterioration and fragmentation of coastal meadows. We sampled DNA across the entire population and used 12 polymorphic microsatellite loci to examine whether the environmental changes have resulted in genetic structuring and loss of variation. RESULTS: We found a pattern of isolation-by-distance across the whole Baltic population and genetic differentiation between local populations, even within the southern Baltic. Observed heterozygosity was lower than expected throughout the range and internal relatedness values were positive indicating inbreeding. CONCLUSIONS: Our results provide long-term, empirical evidence for the theoretically expected links between habitat fragmentation, population subdivision, and gene flow. They also demonstrate a rare case of genetic differentiation between populations of a long-distance migratory species. The Baltic Southern Dunlin differs from many related shorebird species that show near panmixia, reflecting its philopatric life history and the reduced connectivity of its breeding patches. The results have important implications as they suggest that reduced connectivity of breeding habitats can threaten even long-distance migrants if they show strong philopatry during breeding. The Baltic Southern Dunlin warrants urgent conservation efforts that increase functional connectivity and gene flow between breeding areas.

Questing abundance of adult taiga ticks Ixodes persulcatus and their Borrelia prevalence at the north-western part of their distribution.

BACKGROUND: Because ixodid ticks are vectors of zoonotic pathogens, including Borrelia, information of their abundance, seasonal variation in questing behaviour and pathogen prevalence is important for human health. As ticks are invading new areas northwards, information from these new areas are needed. Taiga tick (Ixodes persulcatus) populations have been recently found at Bothnian Bay, Finland. We assessed seasonal variation in questing abundance of ticks and their pathogen prevalence in coastal deciduous forests near the city of Oulu (latitudes 64-65°) in 2019. METHODS: We sampled ticks from May until September by cloth dragging 100 meters once a month at eight study sites. We calculated a density index (individuals/100 m2) to assess seasonal variation. Samples were screened for Borrelia burgdorferi (sensu lato) (including B. afzelii, B. garinii, B. burgdorferi (sensu stricto) and B. valaisana), Borrelia miyamotoi, Anaplasma phagocytophilum, Rickettsia spp., Neoehrlichia mikurensis, Francisella tularensis and Bartonella spp., Babesia spp. and for the tick-borne encephalitis virus. RESULTS: All except one nymph were identified as I. persulcatus. The number of questing adults showed a strong peak in May (median: 6.5 adults/100 m2), which is among the highest values reported in northern Europe, and potentially indicates a large population size. After May, the number of questing adults declined steadily with few adults still sampled in August. Nymphs were present from May until September. We found a striking prevalence of Borrelia spp. in adults (62%) and nymphs (40%), with B. garinii (51%) and B. afzelii (63%) being the most common species. In addition, we found that 26% of infected adults were coinfected with at least two Borrelia genospecies, mainly B. garinii and B. afzelii, which are associated with different host species. CONCLUSIONS: The coastal forest environments at Bothnian Bay seem to provide favourable environments for I. persulcatus and the spread of Borrelia. High tick abundance, a low diversity of the host community and similar host use among larvae and nymphs likely explain the high Borrelia prevalence and coinfection rate. Research on the infestation of the hosts that quantifies the temporal dynamics of immature life stages would reveal important aspects of pathogen circulation in these tick populations.

Effects of male telomeres on probability of paternity in sand lizards.

Standardized swim-up trials are used in in vitro fertilization clinics to select particularly motile spermatozoa in order to increase the probability of a successful fertilization. Such trials demonstrate that sperm with longer telomeres have higher motility and lower levels of DNA damage. Regardless of whether sperm motility, and successful swim-up to fertilization sites, is a direct or correlational effect of telomere length or DNA damage, covariation between telomere length and sperm performance predicts a relationship between telomere length and probability of paternity in sperm competition, a prediction that for ethical reasons cannot be tested on humans. Here, we test this prediction in sand lizards (Lacerta agilis) using experimental data from twice-mated females in a laboratory population, and telomere length in blood from the participating lizards. Female identity influenced paternity (while the mechanism was not identified), while relatively longer male telomeres predicted higher probability of paternity. We discuss potential mechanisms underpinning this result.

Is telomere length associated with mate choice in a songbird with a high rate of extra-pair paternity?

Telomere length is related to aging in many eukaryotes and the rate of telomere attrition has been suggested to reflect individual genetic quality. Telomere length could thus have implications for mate choice. We investigated telomere length variation in bluethroat Luscinia svecica families with mixed paternity, including social parents, extra-pair fathers and nestlings, testing whether telomere length is associated with social and/or extra-pair mate choice through assortative mating or selection of mates with relatively long telomeres. In adults, relative telomere length (rTL) did not differ between the sexes, nor between two age categories. In chicks, however, rTL decreased with body mass at sampling (an index of nestling age). We found a positive correlation between the rTL of social mates, suggesting assortative mating with respect to telomere length or a correlative thereof. However, extra-pair males did not differ from social mates in rTL, and accordingly there was also no difference between within- and extra-pair young (i.e. half-siblings) when controlling for the effect of mass. We found no relationships between telomere length, age and fitness-related traits in adults, but an intriguing year-difference in telomere length in both sexes. In conclusion, we found no support for the idea that females choose extra-pair males based on their telomere length, but social mate choice seems to be influenced by rTL, possibly through its co-variation with aspects reflecting individual quality, like early arrival at the breeding grounds.

Polygamy slows down population divergence in shorebirds.

Sexual selection may act as a promotor of speciation since divergent mate choice and competition for mates can rapidly lead to reproductive isolation. Alternatively, sexual selection may also retard speciation since polygamous individuals can access additional mates by increased breeding dispersal. High breeding dispersal should hence increase gene flow and reduce diversification in polygamous species. Here, we test how polygamy predicts diversification in shorebirds using genetic differentiation and subspecies richness as proxies for population divergence. Examining microsatellite data from 79 populations in 10 plover species (Genus: Charadrius) we found that polygamous species display significantly less genetic structure and weaker isolation-by-distance effects than monogamous species. Consistent with this result, a comparative analysis including 136 shorebird species showed significantly fewer subspecies for polygamous than for monogamous species. By contrast, migratory behavior neither predicted genetic differentiation nor subspecies richness. Taken together, our results suggest that dispersal associated with polygamy may facilitate gene flow and limit population divergence. Therefore, intense sexual selection, as occurs in polygamous species, may act as a brake rather than an engine of speciation in shorebirds. We discuss alternative explanations for these results and call for further studies to understand the relationships between sexual selection, dispersal, and diversification.

Telomere length covaries with personality in wild brown trout.

The prevalence of consistent among-individual differences in behaviour, or personality, makes adaptive sense if individuals differ in stable state variables that shift the balance between the costs and benefits of their behavioural decisions. These differences may give rise to both individual differences in, and covariance among, behaviours that influence an individual's exposure to risks. We here study the link between behaviour and a candidate state variable previously overlooked in the study of state-dependent personality variation: telomere length. Telomeres are the protective endcaps of chromosomes and their erosion with age is thought to play a crucial role in regulating organismal senescence and intrinsic lifespan. Following evidence that shorter telomeres may reduce the lifespan of animals in a wide range of taxa, we predict individuals with shorter telomeres to behave more boldly and aggressively. In order to test this, we measured telomere length and behaviour in wild juvenile brown trout (Salmo trutta). We found individuals with shorter fin telomeres to behave consistently more boldly and aggressively under controlled conditions in the laboratory. No such relationship was found with muscle telomere length 3-4months after the behavioural assays. We suggest that telomere dynamics are an important factor integrating personality traits with other state variables thought to be important in the regulation of behaviour, such as metabolism, disease resistance and growth.

Kin selection and polygyny: can relatedness lower the polygyny threshold?

Resource polygyny incurs costs of having to share breeding resources for female breeders. When breeding with a relative, however, such costs may be lessened by indirect fitness benefits through kin selection, while benefits from mutualistic behaviour, such as communal defence, may increase. If so, females should be less resistant to sharing a territory with a related female than with a non-related one. We investigated whether kin selection may lower the threshold of breeding polygynously, predicting a closer relatedness between polygynous females breeding on the same territory than between females breeding on different territories. Northern lapwings, Vanellus vanellus, are suitable for testing this hypothesis as they are commonly polygynous, both sexes take part in nest defence, and the efficiency of nest defence increases with the number of defenders. Using an index of relatedness derived from DNA fingerprinting, we found that female lapwings that shared polygynous dyads were on average twice as closely related as were random females. Furthermore, relatedness did not correlate with distance between breeders, indicating that our findings cannot be explained by natal philopatry alone. Our results suggest that the polygyny threshold in lapwings may be lowered by inclusive fitness advantages of kin selection.

Rapid growth accelerates telomere attrition in a transgenic fish.

BACKGROUND: Individuals rarely grow as fast as their physiologies permit despite the fitness advantages of being large. One reason may be that rapid growth is costly, resulting for example in somatic damage. The chromosomal ends, the telomeres, are particularly vulnerable to such damage, and telomere attrition thus influences the rate of ageing. Here, we used a transgenic salmon model with an artificially increased growth rate to test the hypothesis that rapid growth is traded off against the ability to maintain somatic health, assessed as telomere attrition. RESULTS: We found substantial telomere attrition in transgenic fish, while maternal half-sibs growing at a lower, wild-type rate seemed better able to maintain the length of their telomeres during the same time period. CONCLUSIONS: Our results are consistent with a trade-off between rapid growth and somatic (telomere) maintenance in growth-manipulated fish. Since telomere erosion reflects cellular ageing, our findings also support theories of ageing postulating that unrepaired somatic damage is associated with senescence.

Telomere dynamics in wild brown trout: effects of compensatory growth and early growth investment.

After a period of food deprivation, animals often respond with a period of faster than normal growth. Such responses have been suggested to result in decreased chromosomal maintenance, which in turn may affect the future fitness of an individual. Here, we present a field experiment in which a food deprivation period of 24 days was enforced on fish from a natural population of juvenile brown trout (Salmo trutta) at the start of the high-growth season in spring. The growth of the food-deprived fish and a non-deprived control group was then monitored in the wild during 1 year. Fin tissue samples were taken at the start of the experiment and 1 year after food deprivation to monitor the telomere dynamics, using reduced telomere length as an indicator of maintenance cost. The food-deprived fish showed partial compensatory growth in both mass and length relative to the control group. However, we found no treatment effects on telomere dynamics, suggesting that growth-compensating brown trout juveniles are able to maintain their telomeres during their second year in the stream. However, body size at the start of the experiment, reflecting growth rate during their first year of life, was negatively correlated with change in telomere length over the following year. This result raises the possibility that rapid growth early in life induces delayed costs in cellular maintenance.

Telomere dynamics in a long-lived bird, the barnacle goose.

BACKGROUND: Theories of ageing predict a trade-off between metabolism, reproduction, and maintenance. Species with low investment in early reproduction are thus expected to be able to evolve more efficient maintenance and repair mechanisms, allowing for a longer potential life span (intrinsic longevity). The erosion of telomeres, the protective caps at the ends of linear chromosomes, plays an important role in cellular and organismal senescence, signalling the onset of age-related disease due to accumulation of unrepaired somatic damage. Using extensive longitudinal data from a long-term study of a natural population of barnacle geese Branta leucopsis, we investigated individual rates of telomere length changes over two years in 34 birds between 0 and 22 years of age, covering almost 80% of the species' lifespan. RESULTS: We show that telomeres in this long-lived bird are very well maintained, as theoretically expected, with an average loss rate of only 5 base pairs per year among adults. We thus found no significant relationship between change in telomere length and age. However, telomeres tended to shorten at a faster pace in juveniles compared to adults. For the first time, we demonstrate a faster telomere attrition rate in females compared to males. We found no correlation between telomere loss rate and adult survival or change in body mass. CONCLUSIONS: Our results add further support for a link between longevity and telomere maintenance, and highlight the complexities of telomere dynamics in natural populations.

Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival.

BACKGROUND: To date, the only estimate of the heritability of telomere length in wild populations comes from humans. Thus, there is a need for analysis of natural populations with respect to how telomeres evolve. METHODOLOGY/PRINCIPAL FINDINGS: Here, we show that telomere length is heritable in free-ranging sand lizards, Lacerta agilis. More importantly, heritability estimates analysed within, and contrasted between, the sexes are markedly different; son-sire heritability is much higher relative to daughter-dam heritability. We assess the effect of paternal age on Telomere Length (TL) and show that in this species, paternal age at conception is the best predictor of TL in sons. Neither paternal age per se at blood sampling for telomere screening, nor corresponding age in sons impact TL in sons. Processes maintaining telomere length are also associated with negative fitness effects, most notably by increasing the risk of cancer and show variation across different categories of individuals (e.g. males vs. females). We therefore tested whether TL influences offspring survival in their first year of life. Indeed such effects were present and independent of sex-biased offspring mortality and offspring malformations. CONCLUSIONS/SIGNIFICANCE: TL show differences in sex-specific heritability with implications for differences between the sexes with respect to ongoing telomere selection. Paternal age influences the length of telomeres in sons and longer telomeres enhance offspring survival.

Sexual differences in telomere selection in the wild.

Telomere length is restored primarily through the action of the reverse transcriptase telomerase, which may contribute to a prolonged lifespan in some but not all species and may result in longer telomeres in one sex than the other. To what extent this is an effect of proximate mechanisms (e.g. higher stress in males, higher oestradiol/oestrogen levels in females), or is an evolved adaptation (stronger selection for telomere length in one sex), usually remains unknown. Sand lizard (Lacerta agilis) females have longer telomeres than males and better maintain telomere length through life than males do. We also show that telomere length more strongly contributes to life span and lifetime reproductive success in females than males and that telomere length is under sexually diversifying selection in the wild. Finally, we performed a selection analysis with number of recruited offspring into the adult population as a response variable with telomere length, life span and body size as predictor variables. This showed significant differences in selection pressures between the sexes with strong ongoing selection in females, with these three predictors explaining 63% of the variation in recruitment. Thus, the sexually dimorphic telomere dynamics with longer telomeres in females is a result of past and ongoing selection in sand lizards. Finally, we compared the results from our selection analyses based on Telometric-derived data to the results based on data generated by the software ImageJ. ImageJ resulted in shorter average telomere length, but this difference had virtually no qualitative effect on the patterns of ongoing selection.

Factors affecting germline mutations in a hypervariable microsatellite: a comparative analysis of six species of swallows (Aves: Hirundinidae).

Microsatellites mutate frequently by replication slippage. Empirical evidence shows that the probability of such slippage mutations may increase with the length of the repeat region as well as exposure to environmental mutagens, but the mutation rate can also differ between the male and female germline. It has been hypothesized that more intense sexual selection or sperm competition can also lead to elevated mutation rates, but the empirical evidence is inconclusive. Here, we analyzed the occurrence of germline slippage mutations in the hypervariable pentanucleotide microsatellite locus HrU10 across six species of swallow (Aves: Hirundinidae). These species exhibit marked differences in the length range of the microsatellite, as well as differences in the intensity of sperm competition. We found a strong effect of microsatellite length on the probability of mutation, but no residual effect of species or their level of sperm competition when the length effect was accounted for. Neither could we detect any difference in mutation rate between tree swallows (Tachycineta bicolor) breeding in Hamilton Harbour, Ontario, an industrial site with previous documentation of elevated mutation rates for minisatellite DNA, and a rural reference population. However, our cross-species analysis revealed two significant patterns of sex differences in HrU10 germline mutations: (1) mutations in longer alleles occurred typically in the male germline, those in shorter alleles in the female germline, and (2) male germline mutations were more often expansions than contractions, whereas no directional bias was evident in the female germline. These results indicate some fundamental differences in male and female gametogenesis affecting the probability of slippage mutations. Our study also reflects the value of a comparative, multi-species approach for locus-specific mutation analyses, through which a wider range of influential factors can be assessed than in single-species studies.

Proximate determinants of telomere length in sand lizards (Lacerta agilis).

Telomeres are repeat sequences of non-coding DNA that cap the ends of chromosomes and contribute to their stability and the genomic integrity of cells. In evolutionary ecology, the main research target regarding these genomic structures has been their role in ageing and as a potential index of age. However, research on humans shows that a number of traits contribute to among-individual differences in telomere length, in particular traits enhancing cell division and genetic erosion, such as levels of free radicals and stress. In lizards, tail loss owing to predation attempts results in a stress-induced shift to a more cryptic lifestyle. In sand lizard (Lacerta agilis) males, telomere length was compromised by tail regrowth in a body size-related manner, so that small males, which already exhibit more cryptic mating tactics, were less affected than larger males. Tail regrowth just fell short of having a significant relationship with telomere length in females, and so did age in males. In females, there was a significant positive relationship between age and telomere length. We conclude that the proximate effect of compromised antipredation and its associated stress seems to have a more pronounced effect in males than in females and that age-associated telomere dynamics differ between the sexes.

Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population.

BACKGROUND: Inbreeding and loss of genetic diversity are expected to increase the extinction risk of small populations, but detailed tests in natural populations are scarce. We combine long-term population and fitness data with those from two types of molecular markers to examine the role of genetic effects in a declining metapopulation of southern dunlins Calidris alpina schinzii, an endangered shorebird. RESULTS: The decline is associated with increased pairings between related individuals, including close inbreeding (as revealed by both field observations of parentage and molecular markers). Furthermore, reduced genetic diversity seems to affect individual fitness at several life stages. Higher genetic similarity between mates correlates negatively with the pair's hatching success. Moreover, offspring produced by related parents are more homozygous and suffer from increased mortality during embryonic development and possibly also after hatching. CONCLUSIONS: Our results demonstrate strong genetic effects in a rapidly declining population, emphasizing the importance of genetic factors for the persistence of small populations.

Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in Great Tits from three different breeding latitudes.

The present study determines how populations of Great Tits (Parus major) breeding in southern, mid and northern European latitudes have adjusted their reproductive endocrinology to differences in the ambient temperature during the gonadal cycle. A study based on long-term breeding data, using the Colwell predictability model, showed that the start of the breeding season has a high predictability ( approximately 0.8-0.9) at all latitudes, and that the environmental information factor (I(e)) progressively decreased from mid Italy (I(e)>4) to northern Finland (I(e)<1). The results indicate that integration of supplementary information, such as ambient temperature, with photoperiodic initial predictive information (day length), becomes progressively more important in maintaining the predictability of the breeding season with decreasing latitude. This hypothesis was verified by exposing photosensitive Great Tits from northern Norway, southern Sweden and northern Italy to sub-maximal photo-stimulatory day lengths (13L:11D) under two different ambient temperature regimes (+4 degrees C and +20 degrees C). Changes in testicular size, plasma levels of LH and testosterone were measured. The main results were: (1) Initial testicular growth rate, as well as LH secretion, was affected by temperature in the Italian, but not in birds from the two Scandinavian populations. (2) Maximum testicular size, maximum LH and testosterone levels were maintained for a progressively shorter period of time with increasing latitude, regardless of whether the birds were kept on a low or a high ambient temperature. (3) In birds from all latitudes, the development of photorefractoriness, as indicated by testicular regression and a decrease in plasma levels of LH and testosterone, started much earlier (with the exception for LH Great Tits from northern Scandinavia) when kept on +20 degrees C than when kept on +4 degrees C. The prolonging effects of a low temperature was more pronounced in Mediterranean birds, than in birds from Scandinavia, and more pronounced in Great Tits from southern Scandinavia than in Great Tits from northern Scandinavia. Ecological implications of the results are discussed, as well as possible impact of global warming on the breeding success of European Great Tits from different breeding latitudes.

Age-independent telomere length predicts fitness in two bird species.

Telomeres are dynamic DNA-protein structures that form protective caps at the ends of eukaryotic chromosomes. Although initial telomere length is partly genetically determined, subsequent accelerated telomere shortening has been linked to elevated levels of oxidative stress. Recent studies show that short telomere length alone is insufficient to induce cellular senescence; advanced attrition of these repetitive DNA sequences does, however, reflect ageing processes. Furthermore, telomeres vary widely in length between individuals of the same age, suggesting that individuals differ in their exposure or response to telomere-shortening stress factors. Here, we show that residual telomere length predicts fitness components in two phylogenetically distant bird species: longevity in sand martins, Riparia riparia, and lifetime reproductive success in dunlins, Calidris alpina. Our results therefore imply that individuals with longer than expected telomeres for their age are of higher quality.

Genetic similarity between mates and extra-pair parentage in three species of shorebirds.

Matings between close relatives often reduce the fitness of offspring, probably because homozygosity leads to the expression of recessive deleterious alleles. Studies of several animals have shown that reproductive success is lower when genetic similarity between parents is high, and that survival and other measures of fitness increase with individual levels of genetic diversity. These studies indicate that natural selection may favour the avoidance of matings with genetically similar individuals. But constraints on social mate choice, such as a lack of alternatives, can lead to pairing with genetically similar mates. In such cases, it has been suggested that females may seek extra-pair copulations with less related males, but the evidence is weak or lacking. Here we report a strong positive relationship between the genetic similarity of social pair members and the occurrence of extra-pair paternity and maternity ('quasi-parasitism') in three species of shorebirds. We propose that extra-pair parentage may represent adaptive behavioural strategies to avoid the negative effects of pairing with a genetically similar mate.

Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus.

Effects of egg size and parental quality on lapwing Vanellus vanellus chick survival were studied in southwestern Sweden over 6 years. Chicks from large eggs were heavier at hatching and survived significantly better than those from small eggs. To control for the confounding effect of parental quality on egg size and chick survival, we performed a cross-fostering experiment during 2 years, exchanging clutches between nests with large and small eggs. In control clutches, chicks from large eggs survived better than those from small eggs, but we found no significant difference in chick survival between exchanged clutches. Thus, egg size did not affect chick survival independently of parental quality. Fledging success increased with parental age and/or experience, and with female body mass. Hence, both egg size and parental quality affect chick survival in the lapwing.