Matthew B Toomey, Kevin J McGraw. 2016: The effects of sun exposure on carotenoid accumulation and oxidative stress in the retina of the House Finch (Haemorhous mexicanus). Avian Research, 7(1): 5. DOI: 10.1186/s40657-016-0041-6
Citation: Matthew B Toomey, Kevin J McGraw. 2016: The effects of sun exposure on carotenoid accumulation and oxidative stress in the retina of the House Finch (Haemorhous mexicanus). Avian Research, 7(1): 5. DOI: 10.1186/s40657-016-0041-6

The effects of sun exposure on carotenoid accumulation and oxidative stress in the retina of the House Finch (Haemorhous mexicanus)

More Information
  • Corresponding author:

    Matthew B.Toomey, mbtoomey@gmail.com

  • Received Date: 04 Sep 2016
  • Accepted Date: 15 Mar 2016
  • Available Online: 24 Apr 2022
  • Publish Date: 28 Mar 2016
  • Background 

    Diet-derived carotenoid pigments are concentrated in the retinas of birds and serve a variety of functions, including photoprotection. In domesticated bird species (e.g., chickens and quail), retinal carotenoid pigmentation has been shown to respond to large manipulations in light exposure and provide protection against photodamage. However, it is not known if or how wild birds respond to ecologically relevant variation in sun exposure.

    Methods 

    We manipulated the duration of natural sunlight exposure and dietary carotenoid levels in wild-caught captive House Finches (Haemorhous mexicanus), then measured carotenoid accumulation and oxidative stress in the retina.

    Results 

    We found no significant effects of sun exposure on retinal levels of carotenoids or lipid peroxidation, in replicate experiments, in winter (Jan–Mar) and spring/summer (May–June). Dietary carotenoid supplementation in the spring/summer experiment led to significantly higher retinal carotenoid levels, but did not affect lipid peroxidation. Carotenoid levels differed significantly between the winter and spring/summer experiments, with higher retinal and lower plasma carotenoid levels in birds from the later experiment.

    Conclusion 

    Our results suggest that variation in the duration of exposure to direct sunlight have limited influence on intraspecific variation in retinal carotenoid accumulation, but that accumulation may track other seasonal–environmental cues and physiological processes.

  • Understanding the origins of organismal diversity is one of the most enduring and important quests in biology. Dispersal is an important intrinsic factor to influence intraspecific divergence and speciation for organisms (Leal et al., 2019; Avaria-Llautureo et al., 2021). According to the intermediate dispersal hypothesis (hereafter, IDH) of species diversity, dispersal has both stimulatory and inhibitory effects on diversification. On one hand, dispersal maintains gene flow and keeps a high level of genetic connectivity among populations (Gavrilets and Vose, 2005), which would inhibit intraspecific genetic differentiation and speciation. On the other hand, higher dispersal ability facilitates species to surmount larger geographic barriers and colonize newly suitable habitats (Hoffmann and Sgrò, 2011; Alzate and Onstein, 2022). Lineages distributed over larger geographical range sizes are prone to subdivision by barriers and further promote intraspecific genetic differentiation and speciation. Thus IDH predicts that lineages with intermediate dispersal abilities experience a blend of range expansion and geographical subdivision that maximizes speciation rates.

    Researches of dispersal on evolutionary divergence have been carried out across a variety of animal taxa, such as arachnids (Luo et al., 2020; Suárez et al., 2022), arthropods (Ortego et al., 2021), reptiles (Sheu et al., 2020), fish (Avaria-Llautureo et al., 2021), birds (Belliure et al., 2000; Claramunt et al., 2012), and mammals (Rolland et al., 2015), and birds were identified as the most frequently studied taxonomic group. The ability of flight endowed by wings, has long been regarded as a hallmark of evolutionary innovation in birds. This adaptation potentially enhances their dispersal capacity to radiate breeding and foraging activities to various areas, contributed to the expansion in genetic divergence and taxonomic diversity. Using hand-wing index (hereafter, HWI), a most commonly proxy for dispersal ability, to measure dispersal ability is widespread in the studies of birds (Lockwood et al., 1998; Claramunt et al., 2012; Sheard et al., 2020; Arango et al., 2022). Meanwhile, previous researches about the influence of dispersal (using by HWI) on evolutionary divergence in birds produced obscure results at both inter-species and intra-species levels (negative correlation: Claramunt et al., 2012; Weeks and Claramunt, 2014; no significant correlation: Kennedy et al., 2016).

    Classical speciation theory proposes that subspecies is a sign of incipient speciation in evolutionary biology (Mayr, 1982; O'Brien and Mayr, 1991; Botero et al., 2014), since speciation in most organisms is initiated via differentiation of populations (Darwin, 1859; O'Brien and Mayr, 1991). Subspecies are defined by phenotypic discontinuities between geographically adjacent or separate populations (Phillimore et al., 2007). Hence, the number of subspecies is tend to represent the degree of intraspecific divergence (Salisbury et al., 2012; Botero et al., 2014; Talavera and Tellería, 2022). In birds, subspecies richness of all species across the world has been described (Clements, 2000; Dickinson, 2003). Although some researchers argued that the number of subspecies may be a conservative representative of intraspecific divergence (Zink, 2004), the overall level of congruence between subspecies and molecular phylogenetic data is great in the description of intraspecific genetic diversity in birds (Phillimore and Owens, 2006). Meanwhile, subspecies richness as an index of recent divergence has been widely used in the researches (Belliure et al., 2000; Mayr and Diamond, 2001; Newton, 2003; Sol et al., 2005; Phillimore et al., 2007; Phillimore et al., 2010; Talavera and Tellería, 2022). In summary, birds represent an ideal system for investigating the relationship between dispersal and intraspecific divergence.

    However, research of this relationship in birds remains scarce, and the sample size is relatively small (Belliure et al., 2000). Birds are one of the most conspicuous and diverse groups of modern vertebrates, and flight is the most remarkable key innovation for it (Hunter, 1998; Brusatte et al., 2015; Crouch and Tobias, 2022). Improving our understanding of the effects of HWI on intraspecific divergence is therefore critical, not only because it provides an excellent opportunity to understand the relationship between life history trait and evolutionary divergence, but it also plays a fundamental role in avian diversity conservation since subspecies is widely used in conservation biology and represents a unit of biological organization (Haig et al., 2006; Braby et al., 2012).

    Here, we investigate the influence of dispersal on intraspecific divergence (assessed as number of subspecies) across bird species in the world. The study system has three major advantages in addressing this issue. First, by assessing the relationship between dispersal and evolutionary divergence at a global scale (7092 species), we will obtain a broader perspective, since relatively small sample size may bias the result of study. Second, we use the HWI to quantify the dispersal ability, for which HWI has been proved to be a good proxy (Dawideit et al., 2009; Claramunt et al., 2012; Weeks and Claramunt, 2014; Pigot and Tobias, 2015; Kennedy et al., 2016; Stoddard et al., 2017; Sheard et al., 2020; Arango et al., 2022). Third, ecological factors, such as temperature and precipitation, play a key role in avian intraspecific divergence (Botero et al., 2014; Condamine et al., 2019). In this study we will control for these ecological factors that have often been overlooked in previous studies.

    We obtained the data on subspecies richness of species and climate (annual temperature and precipitation) within a species' range from Botero et al. (2014), and data for HWI were obtained from Sheard et al. (2020). We also collected information about diet, habitat, association with islands, body mass, and range size for each species from Sheard et al. (2020). We assigned each species as being herbivorous (fruit, seeds, nectar, plants), carnivorous (invertebrates, vertebrates, scavenger), or omnivorous. Each species was classified into one of the habitat types: open (desert, grassland, open water, low shrubs, rocky habitats, seashores, and cities), semi-open (open shrub land, scattered bushes, parkland, dry or deciduous forest, thorn forest), and dense (tall evergreen forest with a closed canopy, or in the lower vegetation strata of dense thickets, shrubland or marshland), for details see Tobias et al. (2016). Association with islands is a variable that quantifies the proportion of islands in the distribution range (Sheard et al., 2020).

    We employed Markov chain Monte Carlo generalized linear mixed models (MCMCglmm) to test whether intraspecific divergence was associated with HWI, and flightless birds (Sayol et al., 2020) were removed from the dataset before analysis. In any interspecific comparative analysis, a key statistical issue is that the species compared are not independent since they share a common evolutionary history. Hence, a tree describing the evolutionary relationship among the sampled species was used to solve the non-independence problem (e.g., Chen et al., 2021; Liu et al., 2023; Li et al., 2024). The phylogenetic tree used in this study was a consensus tree based on 1000 trees that were downloaded from http://birdtree.org (Jetz et al., 2012). Analyses were conducted using the MCMCglmm package (Hadfield, 2010). We ran each model with 300, 000 iterations, 2000 burn-in, and thinning of 50 to ensure satisfactory convergence. Convergence was confirmed by examining the plots of chain mixing and the degree of autocorrelation, a commonly used method for convergence diagnosis (e.g., Wang and Lu, 2018; Li et al., 2024).

    For each model, we included diet, habitat, body mass, association with islands, range size, and climate to control for their potential impact on the response variables. Diet is thought to be a evolutionary force for the divergence of species (Burin et al., 2016). Habitat is related with the number of subspecies in species (Dingle et al., 2008). Body mass is an important life history trait that affects the number of subspecies (Phillimore et al., 2007; Botero et al., 2014). Island species has a higher speciation rate than the mainland species (Hastings and Gavrilets, 1999). Migration status was not included in the model given that migratory behavior is closely associated with HWI (Kennedy et al., 2016). Species with strong dispersal ability is often assumed to promote range expansion by facilitating the colonization of new areas, thereby promoting evolutionary divergence. However, the empirical evidence linking dispersal ability to range size is obscure (Alzate and Onstein, 2022). Although a recent study showed that a weak positive correlation existed between HWI and range size in birds, the study inappropriately included flightless birds (Sheard et al., 2020). Hence, we added range size as a control variable in the final model, and the variance inflation factors (VIF) of all independent variables were less than 2, indicating that no collinearity existed among variables included in the model (Montgomery et al., 2012). In addition, we also tested whether a quadratic correlation existed between HWI and number of subspecies by using MCMCglmm model.

    All analyses were performed with R software (R Core Team, 2022), and phylogenetic tree was drawn on https://www.chiplot.online/. All values given were mean ± standard error (S.E.). Prior to analyses, association with islands was arcsine transformed and all other continuous independent variables were standardized (scaled to a mean of 0 and a variance of 1) to meet the assumptions required for linear regressions.

    Our data set consists of 7092 species (1787 genera, 200 families, and 28 orders; Fig. 1; Appendix Table S1). The number of subspecies ranged from 1 to 73 (3.01 ± 0.04), HWI ranged from 0.07 to 74.80 (25.60 ± 0.17), body mass ranged from 1.90 to 11, 236.10 g (234.00 ± 8.50 g), range size ranged from 1 to 6303 km2 (275.85 ± 5.67 km2), association with islands ranged from 0 to 1 (0.13 ± 0.003), annual temperature ranged from −15.36 to 28.14 ℃ (20.00 ± 0.09 ℃), and annual precipitation ranged from 12.24 to 5321.25 mm (1543.53 ± 9.78 mm).

    Figure  1.  The phylogenetic distribution of 7092 bird species in the study. For aesthetic purposes and to avoid skew from extreme outlier data, the number of subspecies was set to 10 for species that contain more than 10 subspecies (n = 272, 3.8%); the score of speciation rate was set to 1 for species whose speciation rates were larger than 1 (n = 58, 0.6%); and the score of HWI was set to 60 for species whose HWI was larger than 60 (n = 516, 5.4%). HWI: hand-wing index; SR: speciation rate; NOS: number of subspecies.

    The MCMCglmm analyses demonstrate that a significant negative relationship exists between the HWI and number of subspecies among 7092 bird species, after correcting for body mass, range size, climate factors, association with islands, diet and habitat type (Table 1; Fig. 2). In addition, a significant negative correlation between body mass and subspecies richness was noted (Table 1; Fig. 2). We also detected a significant positive effect of range size on variation in the number of subspecies, that is, subspecies richness was higher in species with a widespread distribution range (Table 1, Fig. 2). Our analyses revealed that annual temperature significantly predicted interspecific variation in subspecies richness, whereas annual precipitation did not (Table 1, Fig. 2). Species inhabiting an island-like habitat had lower subspecies richness (Table 1, Fig. 2). The subspecies richness of omnivorous species was higher than that of carnivorous species, while there was no significant difference in subspecies richness between herbivorous and carnivorous species (Table 1, Fig. 2). Open-habitat species appeared to have a lower subspecies number than dense-habitat species, while the species in the semi-open habitat have no significant difference from the ones in dense habitat (Table 1, Fig. 2).

    Table  1.  MCMCglmm model analyses to investigate whether variation in number of subspecies depended on hand-wing index (HWI) across 7092 bird species in the world, controlling for the effect of several confounding factors. Statistically significant variables are highlighted in bold.
    Estimate Lower CI Upper CI Effective sample PMCMC
    Intercept 0.734 0.468 1.021 5960 < 0.001
    Hand-wing index −0.060 −0.107 −0.014 6872 0.012
    Body mass −0.109 −0.149 −0.070 5960 < 0.001
    Range size 0.345 0.326 0.365 5656 < 0.001
    Annual temperature 0.079 0.051 0.108 5960 < 0.001
    Annual precipitation 0.014 −0.014 0.044 5960 0.350
    Association with islands −0.125 −0.183 −0.070 5197 < 0.001
    Diet: herbivore 0.000 −0.072 0.071 5960 0.995
    Diet: omnivore 0.093 0.018 0.162 5960 0.013
    Habitat: open −0.104 −0.178 −0.026 5960 0.006
    Habitat: semi-open 0.005 −0.044 0.057 5960 0.828
     | Show Table
    DownLoad: CSV
    Figure  2.  Coefficient estimates of models predicting number of subspecies. Coefficient estimates of models considering hand-wing index (HWI), body mass, range size, annual temperature, annual precipitation, association with islands, diet, habitat as predictors, while controlling for phylogenetic effects (for details see Table 1). A negative effect means that the predictor reduces intraspecific divergence.

    Moreover, we also tested whether a quadratic correlation existed between HWI and number of subspecies, and the results of repeated analyses showed that no quadratic correlation was found, and the correlations between the control variables and subspecies richness were highly consistent (Table 2).

    Table  2.  MCMCglmm model analyses to investigate whether a quadratic correlation exists between hand-wing index (HWI) and number of subspecies. Statistically significant variables are highlighted in bold.
    Empty Cell Estimate Lower CI Upper CI Effective sample PMCMC
    Intercept 0.732 0.438 0.990 5960 < 0.001
    Hand-wing index −0.027 −0.153 0.094 5960 0.683
    (Hand-wing index)2 −0.039 −0.177 0.095 5960 0.587
    Body mass −0.110 −0.149 −0.069 5811 < 0.001
    Range size 0.345 0.325 0.366 5560 < 0.001
    Annual temperature 0.080 0.051 0.108 5960 < 0.001
    Annual precipitation 0.014 −0.016 0.043 5569 0.365
    Association with islands −0.124 −0.183 −0.068 5662 < 0.001
    Diet: herbivore −0.002 −0.074 0.067 5960 0.980
    Diet: omnivore 0.091 0.020 0.163 5906 0.011
    Habitat: open −0.104 −0.179 −0.028 5643 0.008
    Habitat: semi-open 0.006 −0.045 0.058 7616 0.817
     | Show Table
    DownLoad: CSV

    In this study, we found that strong dispersal ability is associated with low subspecies richness across 7092 avian species. To our knowledge, this is the first study to examine the effect of dispersal ability on subspecies richness on a global scale in birds. HWI is a phenotypic trait that exerts significant influence on avian dispersal, and subspecies is an important conception in speciation theory and conservation biology. Investigating, hence, the effect of HWI on subspecies richness would not only broaden our understanding of the association between morphological traits and evolutionary divergence in birds, but also contribute to the conservation of avian species diversity.

    Our results may support the scenario that species with low HWI have low dispersal ability and less gene flow between populations, then morphological and molecular differences would be easy to form. If geographic barriers to lower dispersal ability were semipermeable, that is, if dispersal across a barrier is possible but difficult, then reduced gene flow would allow for divergence in some important traits such as sexual signals even without strong selection for local ecological adaptation (Uy et al., 2018). This result is consistent with results of previous studies carried out at both population (Crochet, 2000) and species (Belliure et al., 2000; Claramunt et al., 2012; Weeks and Claramunt, 2014) levels in birds.

    Meanwhile, no quadratic correlation exists between HWI and subspecies richness in our study, which is consistent with previous studies that demonstrated that a quadratic model is not better than linear model to describe the relationship between dispersal ability and subspecies richness (Claramunt et al., 2012; Weeks and Claramunt, 2014; Kennedy et al., 2016). According to the intermediate dispersal hypothesis (hereafter, IDH), the unimodal relationship between dispersal ability and diversification is associated by the fact that dispersal could increase gene flow to inhibit differentiation and increase range expansion to promote differentiation. However, little evidence could be found in previous studies to support the latter view, despite range expansion may play an important role in diversification (Milá et al., 2007). Our results showed a significant positive correlation between range size and subspecies richness. For birds, the relative impacts of gene flow and range expansion due to dispersal may be more significant than for other animals because of their ability to fly. However, we did not observe a colinearity between range size and HWI, which means no strong correlation between them at the global scale in birds. Meanwile, existing studies also still provide limited evidence for a correlation between distributional range and HWI (Alzate and Onstein, 2022). After accounting for the potentially stimulating effects of colonization and range expansion, the inhibitory effect of increased levels of gene flow endowed by high HWI on the number of subspecies in bird is still significant. Therefore, these results suggest that stronger gene flow induced by higher HWI significantly reduced the degree of intraspecific divergence and isolation remains an important driver of intraspecific genetic divergence in birds.

    However, some researchers believe that when more bird species are included, the unimodal relationship between HWI and diversification may be easier to appear (Tobias et al., 2020). We failed to verify this hypothesis by using almost all bird species in the world, which indicate that using HWI to measure dispersal ability may not effectively test IDH in birds (Alzate and Onstein, 2022). On one hand, HWI as a measurement of dispersal ability may not effectively represent the range expansion capacity of bird species. The 'transporter' hypothesis predicts that birds may experience repeated losses of dispersal in 'insular' habitats (e.g., island and alpine ecosystems), which means the variation in wing morphology may obscure this pattern. For example, reduced dispersal ability may be selected after lineages with moderate dispersal capacity colonized islands (Leisler and Winkler, 2015; Kennedy et al., 2016; Hosner et al., 2017). On the other hand, strong dispersal ability is helpful but not sufficient to drive the completion of speciation cycle of birds (Tobias et al., 2020). Hence, we should be cautious when using HWI to verify the IDH, despite HWI is a commonly proxy for flight efficiency and dispersal ability as it affects dispersal distances and decreases population geographical isolation and spatial genetic differentiation in birds (Pigot and Tobias, 2015; Sheard et al., 2020; Alzate and Onstein, 2022). Nevertheless, our study does not deny that the IDH may be verified at intra-species or other levels. IDH can still help us to understand and predict current biological patterns since it provides a conceptual link to analyze the evolutionary cost/benefit of dispersal ability and its impact on species diversity, but a better exploration of indicators for dispersal agents and diversity indices is needed.

    In addition, our comparative analyses revealed that body mass is significantly linked to subspecies richness, which is consistent with previous researches (Belliure et al., 2000; Botero et al., 2014). The results also showed that the larger geographical range is associated with higher subspecies richness across bird species, which is probably because a widespread distribution range can lead to population differentiation due to different local selective pressures (Belliure et al., 2000; Phillimore et al., 2007). The annual temperature is positively associated with subspecies richness, which is consistent with the argument that higher temperatures cause shorter generation times, faster mutation rates and hence higher rates of diversification (Rohde, 1992). The subspecies richness of omnivores is higher than that of carnivores, possibly due to that the former occupies larger range size (Galiana et al., 2023). Species in dense habitats possess higher subspecies richness than those in open habitats, presumably because dispersal limitation drives allopatric divergence by restricting gene flow between populations.

    Dispersal plays an important role in the conservation and recovery of wild populations under habitat fragmentation and loss (Smith et al., 2014; Kennedy et al., 2016). Meanwhile, dispersal traits can help us move towards an in-depth understanding of how species respond to climate and land-use changes (Travis et al., 2013; Bregman et al., 2014). In addition, subspecies is widely used in conservation biology since it represents a unit of biological organization (Haig et al., 2006; Braby et al., 2012). Especially in the absence of molecular data, the conservation utility of subspecies becomes more important because subspecies provides an effective way to estimate intraspecific genetic diversity (Phillimore and Owens, 2006). Therefore, in the context of biodiversity loss caused by human activities, the negative correlation between dispersal ability and subspecies richness will provide a theoretical basis for the formulation of bird species diversity conservation strategies.

    Haiying Fan: Writing – original draft, Formal analysis, Data curation. Weibin Guo: Writing – original draft, Formal analysis, Data curation. Buge Lin: Investigation, Data curation. Zhiqing Hu: Investigation, Data curation. Changcao Wang: Writing – review & editing, Writing – original draft, Investigation, Conceptualization. Shaobin Li: Writing – review & editing, Investigation, Conceptualization.

    The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

    We thank Hongtao Xiao for helpful suggestions on statistical analyses.

    Supplementary data to this article can be found online at https://doi.org/10.1016/j.avrs.2024.100188.

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