We genetically analysed malaria parasites (Protozoa) in three Mediterranean blue tit (Cyanistes c... more We genetically analysed malaria parasites (Protozoa) in three Mediterranean blue tit (Cyanistes caeruleus) populations from central Spain. A total of 853 breeding individuals were screened for parasites of the genera Plasmodium and Haemoproteus using a very efficient polymerase chain reaction approach that amplifies a partial segment of the mitochondrial cytochrome b gene of these parasites. We have found six lineages of Plasmodium (SGS1, GRW11, COLL1, DELURB4, GRW04 and BLUTI10) parasitizing the studied populations but we did not detect any infection by Haemoproteus. One of the detected lineages (BLUTI10) has not been previously described in any bird species and this is the first study recording lineages DELURB4 and GRW04 in blue tits. SGS1 (belonging to the morphospecies Plasmodium relictum) was the most frequent lineage (overall prevalence, 24 %), whereas the other lineages showed a much lower prevalence (<4 %). Only a small proportion (12.2 %) of positive amplifications of the most common lineage (SGS1) was detected in blood smears using light microscopy and infection intensities were very low (mean ±SE, 2.0±1.4 parasites/2,000 erythrocytes). We have also found strong inter-population variability in prevalence patterns (12-41 % for lineage SGS1), suggesting important differences in parasite transmission rates among the geographically close studied localities.
In natural populations, mating between relatives can have important fitness consequences due to t... more In natural populations, mating between relatives can have important fitness consequences due to the negative effects of reduced heterozygosity. Parental level of inbreeding or heterozygosity has been also found to influence the performance of offspring, via direct and indirect parental effects that are independent of the progeny own level of genetic diversity. In this study, we first analysed the effects of parental heterozygosity and relatedness (i.e. an estimate of offspring genetic diversity) on four traits related to offspring viability in great tits (Parus major) using 15 microsatellite markers. Second, we tested whether significant heterozygosity-fitness correlations (HFCs) were due to 'local' (i.e. linkage to genes influencing fitness) and/or 'general' (genome-wide heterozygosity) effects. We found a significant negative relationship between parental genetic relatedness and hatching success, and maternal heterozygosity was positively associated with offspring body size. The characteristics of the studied populations (recent admixture, polygynous matings) together with the fact that we found evidence for identity disequilibrium across our set of neutral markers suggest that HFCs may have resulted from genome-wide inbreeding depression. However, one locus (Ase18) had disproportionately large effects on the observed HFCs: heterozygosity at this locus had significant positive effects on hatching success and offspring size. It suggests that this marker may lie near to a functional locus under selection (i.e. a local effect) or, alternatively, heterozygosity at this locus might be correlated to heterozygosity across the genome due to the extensive ID found in our populations (i.e. a general effect). Collectively, our results lend support to both the general and local effect hypotheses and reinforce the view that HFCs lie on a continuum from inbreeding depression to those strictly due to linkage between marker loci and genes under selection.
Dispersal and local patterns of adaptation play a major role on the ecological and evolutionary t... more Dispersal and local patterns of adaptation play a major role on the ecological and evolutionary trajectory of natural populations. In this study, we employ a combination of genetic (25 microsatellite markers) and field-based information (seven study years) to analyse the impact of immigration and local patterns of adaptation in two nearby (<7 km) blue tit (Cyanistes caeruleus) populations. We used genetic assignment analyses to identify immigrant individuals and found that dispersal rate is female-biased (72%). Data on lifetime reproductive success indicated that immigrant females produced fewer local recruits than their philopatric counterparts whereas immigrant males recruited more offspring than those that remained in their natal location. In spite of the considerably higher immigration rates of females, our results indicate that, in absolute terms, their demographic and genetic impact in the receiving populations is lower than that in immigrant males. Immigrants often brought...
Proceedings of the Royal Society B: Biological Sciences, 2009
The general hypothesis of mate choice based on non-additive genetic traits suggests that individu... more The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatednessbased mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner's heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the broodrearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.
The frequency of extrapair paternity within populations has been hypothesized to be related to ec... more The frequency of extrapair paternity within populations has been hypothesized to be related to ecological and social factors, which in turn can determine the impact of extrapair paternity on the opportunity for sexual selection. Here, we use the blue tit Cyanistes caeruleus as study species to assess both issues. In particular, we analyze patterns of extrapair paternity in 12 nest-box plots that greatly vary in local population size, level of nest-box aggregation, and breeding density. We found a significant positive relationship between extrapair paternity rate and local population size. Within study plots, neither local breeding density nor synchrony had an effect on the occurrence of extrapair paternity. Most extrapair males engaged in extrapair copulations with neighbouring females, probably in order to avoid paternity losses. Individuals that travelled larger distances to gain extrapair paternity likely did so because the social females of most of them had not yet begun their fertile period and, thus, within-pair paternity was not at risk. Variance in male reproductive success was mostly produced by variance in within-pair success, which in turn was primarily influenced by mate quality. Extrapair success contributed substantially to variance in male reproductive success (26%), but its effect was smaller than expected. Bateman gradients showed positive slopes (β ss ) for both males and females. However, the lack of a positive covariance between within-pair and extrapair success suggests that the effect of extrapair paternity on the strength of sexual selection was limited. This fact can be explained by the spatial distribution of extrapair fertilizations, which points to the absence of directional female mating preferences in this study system and, thus, not leading to "big winners" and "big losers."
Understanding the importance of host genetic diversity for coping with parasites and infectious d... more Understanding the importance of host genetic diversity for coping with parasites and infectious diseases is a long-standing goal in evolutionary biology. Here, we study the association between probability of infection by avian malaria (Plasmodium relictum) and individual genetic diversity in three blue tit (Cyanistes caeruleus) populations that strongly differ in prevalence of this parasite. For this purpose, we screened avian malaria infections and genotyped 789 blue tits across 26 microsatellite markers. We used two different arrays of markers: 14 loci classified as neutral and 12 loci classified as putatively functional. We found a significant relationship between probability of infection and host genetic diversity estimated at the subset of neutral markers that was not explained by strong local effects and did not differ among the studied populations. This relationship was not linear, and probability of infection increased up to values of homozygosity by locus (HL) around 0.15, reached a plateau at values of HL from 0.15 to 0.40 and finally declined among a small proportion of highly homozygous individuals (HL > 0.4). We did not find evidence for significant identity disequilibrium, which may have resulted from a low variance of inbreeding in the study populations and/or the small power of our set of markers to detect it. A combination of subtle positive and negative local effects and/or a saturation threshold in the association between probability of infection and host genetic diversity in combination with increased resistance to parasites in highly homozygous individuals may explain the observed negative quadratic relationship. Overall, our study highlights that parasites play an important role in shaping host genetic variation and suggests that the use of large sets of neutral markers may be more appropriate for the study of heterozygosity-fitness correlations.
The genus Apteromantis Werner, 1931 comprises two species of wingless mantids, the Iberian A. apt... more The genus Apteromantis Werner, 1931 comprises two species of wingless mantids, the Iberian A. aptera (Fuente, 1894) and the North African A. bolivari (Werner, 1929). Although A. aptera and A. bolivari have been traditionally considered as separate and valid species, their external appearance is quite similar and no comprehensive taxonomic study has analyzed their morphological and genetic characteristics. This taxonomic uncertainty has important implications for conservation because A. aptera is considered an Iberian endemic and the only praying mantis protected by international laws. In this study, we apply a comprehensive approach, including quantitative morphological and molecular analyses, to shed new light on the taxonomic and conservation status of the genus Apteromantis and the putative species. We have found that the Iberian and North African specimens analyzed herein significantly differ in female head shape, male genitalia morphology and several other traits related to body size. Molecular data suggest the presence of two main lineages, with sequence divergence rates of approximately 4 %, which are within the range reported for other well defined insect species. Overall, this study supports that A. aptera and A. bolivari are valid species despite their ecological and morphological similarity and highlights the importance of comprehensive approaches to resolve old taxonomic and conservation problems.
We genetically analysed malaria parasites (Protozoa) in three Mediterranean blue tit (Cyanistes c... more We genetically analysed malaria parasites (Protozoa) in three Mediterranean blue tit (Cyanistes caeruleus) populations from central Spain. A total of 853 breeding individuals were screened for parasites of the genera Plasmodium and Haemoproteus using a very efficient polymerase chain reaction approach that amplifies a partial segment of the mitochondrial cytochrome b gene of these parasites. We have found six lineages of Plasmodium (SGS1, GRW11, COLL1, DELURB4, GRW04 and BLUTI10) parasitizing the studied populations but we did not detect any infection by Haemoproteus. One of the detected lineages (BLUTI10) has not been previously described in any bird species and this is the first study recording lineages DELURB4 and GRW04 in blue tits. SGS1 (belonging to the morphospecies Plasmodium relictum) was the most frequent lineage (overall prevalence, 24 %), whereas the other lineages showed a much lower prevalence (<4 %). Only a small proportion (12.2 %) of positive amplifications of the most common lineage (SGS1) was detected in blood smears using light microscopy and infection intensities were very low (mean ±SE, 2.0±1.4 parasites/2,000 erythrocytes). We have also found strong inter-population variability in prevalence patterns (12-41 % for lineage SGS1), suggesting important differences in parasite transmission rates among the geographically close studied localities.
In natural populations, mating between relatives can have important fitness consequences due to t... more In natural populations, mating between relatives can have important fitness consequences due to the negative effects of reduced heterozygosity. Parental level of inbreeding or heterozygosity has been also found to influence the performance of offspring, via direct and indirect parental effects that are independent of the progeny own level of genetic diversity. In this study, we first analysed the effects of parental heterozygosity and relatedness (i.e. an estimate of offspring genetic diversity) on four traits related to offspring viability in great tits (Parus major) using 15 microsatellite markers. Second, we tested whether significant heterozygosity-fitness correlations (HFCs) were due to 'local' (i.e. linkage to genes influencing fitness) and/or 'general' (genome-wide heterozygosity) effects. We found a significant negative relationship between parental genetic relatedness and hatching success, and maternal heterozygosity was positively associated with offspring body size. The characteristics of the studied populations (recent admixture, polygynous matings) together with the fact that we found evidence for identity disequilibrium across our set of neutral markers suggest that HFCs may have resulted from genome-wide inbreeding depression. However, one locus (Ase18) had disproportionately large effects on the observed HFCs: heterozygosity at this locus had significant positive effects on hatching success and offspring size. It suggests that this marker may lie near to a functional locus under selection (i.e. a local effect) or, alternatively, heterozygosity at this locus might be correlated to heterozygosity across the genome due to the extensive ID found in our populations (i.e. a general effect). Collectively, our results lend support to both the general and local effect hypotheses and reinforce the view that HFCs lie on a continuum from inbreeding depression to those strictly due to linkage between marker loci and genes under selection.
Dispersal and local patterns of adaptation play a major role on the ecological and evolutionary t... more Dispersal and local patterns of adaptation play a major role on the ecological and evolutionary trajectory of natural populations. In this study, we employ a combination of genetic (25 microsatellite markers) and field-based information (seven study years) to analyse the impact of immigration and local patterns of adaptation in two nearby (<7 km) blue tit (Cyanistes caeruleus) populations. We used genetic assignment analyses to identify immigrant individuals and found that dispersal rate is female-biased (72%). Data on lifetime reproductive success indicated that immigrant females produced fewer local recruits than their philopatric counterparts whereas immigrant males recruited more offspring than those that remained in their natal location. In spite of the considerably higher immigration rates of females, our results indicate that, in absolute terms, their demographic and genetic impact in the receiving populations is lower than that in immigrant males. Immigrants often brought...
Proceedings of the Royal Society B: Biological Sciences, 2009
The general hypothesis of mate choice based on non-additive genetic traits suggests that individu... more The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatednessbased mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner's heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the broodrearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.
The frequency of extrapair paternity within populations has been hypothesized to be related to ec... more The frequency of extrapair paternity within populations has been hypothesized to be related to ecological and social factors, which in turn can determine the impact of extrapair paternity on the opportunity for sexual selection. Here, we use the blue tit Cyanistes caeruleus as study species to assess both issues. In particular, we analyze patterns of extrapair paternity in 12 nest-box plots that greatly vary in local population size, level of nest-box aggregation, and breeding density. We found a significant positive relationship between extrapair paternity rate and local population size. Within study plots, neither local breeding density nor synchrony had an effect on the occurrence of extrapair paternity. Most extrapair males engaged in extrapair copulations with neighbouring females, probably in order to avoid paternity losses. Individuals that travelled larger distances to gain extrapair paternity likely did so because the social females of most of them had not yet begun their fertile period and, thus, within-pair paternity was not at risk. Variance in male reproductive success was mostly produced by variance in within-pair success, which in turn was primarily influenced by mate quality. Extrapair success contributed substantially to variance in male reproductive success (26%), but its effect was smaller than expected. Bateman gradients showed positive slopes (β ss ) for both males and females. However, the lack of a positive covariance between within-pair and extrapair success suggests that the effect of extrapair paternity on the strength of sexual selection was limited. This fact can be explained by the spatial distribution of extrapair fertilizations, which points to the absence of directional female mating preferences in this study system and, thus, not leading to "big winners" and "big losers."
Understanding the importance of host genetic diversity for coping with parasites and infectious d... more Understanding the importance of host genetic diversity for coping with parasites and infectious diseases is a long-standing goal in evolutionary biology. Here, we study the association between probability of infection by avian malaria (Plasmodium relictum) and individual genetic diversity in three blue tit (Cyanistes caeruleus) populations that strongly differ in prevalence of this parasite. For this purpose, we screened avian malaria infections and genotyped 789 blue tits across 26 microsatellite markers. We used two different arrays of markers: 14 loci classified as neutral and 12 loci classified as putatively functional. We found a significant relationship between probability of infection and host genetic diversity estimated at the subset of neutral markers that was not explained by strong local effects and did not differ among the studied populations. This relationship was not linear, and probability of infection increased up to values of homozygosity by locus (HL) around 0.15, reached a plateau at values of HL from 0.15 to 0.40 and finally declined among a small proportion of highly homozygous individuals (HL > 0.4). We did not find evidence for significant identity disequilibrium, which may have resulted from a low variance of inbreeding in the study populations and/or the small power of our set of markers to detect it. A combination of subtle positive and negative local effects and/or a saturation threshold in the association between probability of infection and host genetic diversity in combination with increased resistance to parasites in highly homozygous individuals may explain the observed negative quadratic relationship. Overall, our study highlights that parasites play an important role in shaping host genetic variation and suggests that the use of large sets of neutral markers may be more appropriate for the study of heterozygosity-fitness correlations.
The genus Apteromantis Werner, 1931 comprises two species of wingless mantids, the Iberian A. apt... more The genus Apteromantis Werner, 1931 comprises two species of wingless mantids, the Iberian A. aptera (Fuente, 1894) and the North African A. bolivari (Werner, 1929). Although A. aptera and A. bolivari have been traditionally considered as separate and valid species, their external appearance is quite similar and no comprehensive taxonomic study has analyzed their morphological and genetic characteristics. This taxonomic uncertainty has important implications for conservation because A. aptera is considered an Iberian endemic and the only praying mantis protected by international laws. In this study, we apply a comprehensive approach, including quantitative morphological and molecular analyses, to shed new light on the taxonomic and conservation status of the genus Apteromantis and the putative species. We have found that the Iberian and North African specimens analyzed herein significantly differ in female head shape, male genitalia morphology and several other traits related to body size. Molecular data suggest the presence of two main lineages, with sequence divergence rates of approximately 4 %, which are within the range reported for other well defined insect species. Overall, this study supports that A. aptera and A. bolivari are valid species despite their ecological and morphological similarity and highlights the importance of comprehensive approaches to resolve old taxonomic and conservation problems.
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Papers by Joaquín Ortego