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Identification of novel genetic loci related to dromedary camel (Camelus dromedarius) morphometrics, biomechanics, and behavior by genome-wide association studies

BMC Veterinary Research volume 20, Article number: 418 (2024) Cite this article

Abstract

In the realm of animal breeding for sustainability, domestic camels have traditionally been valued for their milk and meat production. However, key aspects such as zoometrics, biomechanics, and behavior have often been overlooked in terms of their genetic foundations. Recognizing this gap, the present study perfomed genome-wide association analyses to identify genetic markers associated with zoometrics-, biomechanics-, and behavior-related traits in dromedary camels (Camelus dromedarius). 16 and 108 genetic markers were significantly associated (q < 0.05) at genome and chromosome-wide levels of significance, respectively, with zoometrics- (width, length, and perimeter/girth), biomechanics- (acceleration, displacement, spatial position, and velocity), and behavior-related traits (general cognition, intelligence, and Intelligence Quotient (IQ)) in dromedaries. In most association loci, the nearest protein-coding genes are linkedto neurodevelopmental and sensory disorders. This suggests that genetic variations related to neural development and sensory perception play crucial roles in shaping a dromedary camel’s physical characteristics and behavior. In summary, this research advances our understanding of the genomic basis of essential traits in dromedary camels. Identifying specific genetic markers associated with zoometrics, biomechanics, and behavior provides valuable insights into camel domestication. Moreover, the links between these traits and genes related to neurodevelopmental and sensory disorders highlight the broader implications of domestication and modern selection on the health and welfare of dromedary camels. This knowledge could guide future breeding strategies, fostering a more holistic approach to camel husbandry and ensuring the sustainability of these animals in diverse agricultural contexts.

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Background

Recognized for their sustainability, domestic camels (dromedaries or one-humped camels (Camelus dromedarius) and Bactrian or two-humped camels (Camelus bactrianus)) are increasingly raised for various productive purposes worldwide. With a notable demand for camel milk and meat, efforts and strategies focus on growth and milk yield traits. This often sidelines traits like zoometrics, biomechanics, and behavior in genetic improvement programs for these animals [1, 2]. Therefore, standardizing the incorporation of these traits into breeding criteria—linked to physical and behavioral performance—will enhance the potential of camels. This is especially relevant for camel breeds and populations used in beauty contests, athletic pursuits (racing and riding), and close interaction with humans (assisted interventions and routine husbandry practices) [3, 4].

In conservation and/or breeding programs, two essential data registries are crucial: phenotypic records of the traits of interest and genealogical information [5]. Estimating individual breeding values using phenotypic and pedigree information is limited for camels due to the lack of traditional pedigrees [6, 7]. To overcome this technical constraint and enhance genetic advancement, efforts are being made to reduce generation intervals [8], which can be achieved by implementing genomics-based selection programs.

Progress in genomic research has provided powerful tools forexamining the genetic composition of complex traits and developing selection panels based on genetic markers. This includes single-gene tests [9] and more complex arrays of genetic markers spanning the entire genome, which are known to correlate with specific traits [10]. Genetic polymorphisms of single candidate genes have been proposed in dromedary camels for economically relevant traits such as coat colour [11], udder and body measurements [12,13,14], and reproductive performance [15].

Complex genetic breeding programs can also be developed using genome-wide association studies (GWAS). For instance, Bitaraf Sani, Zare Harofte [6] identified 99 genome-wide significant SNPs associated with birth weight, daily gain, and body weight in Iranian dromedaries. Within the same animal population, 9 significant SNPs located in 16 candidate genes and 13 significant SNPs located in 24 candidate genes were associated with white and black coat color, respectively [16]. Additionally, Karimi, Burger [17] found 59 SNPs significantly associated with 12 morphometric traits and classified 37 candidate genes in Iranian dromedaries. Moreover, 111 SNPs were identified as significantly associated with weight-for-age traits in Pakistani dromedary camels [18].

However, the genetic basis of other functional traits of economic relevance, such as athletic performance and behavioural features, remains unexplored [19]. From an evolutionary perspective, identifying genomic regions associated with specific phenotypic traits can help disentangle the effects of early domestication and historical selective breeding on camel health and welfare, based on the biological functions of the associated genes (‘domestication syndrome’ hypothesis) [20].

The present study performs genome-wide association studies to identify genomic regions that may regulate the expression of traits such as zoometrics, biomechanics, and behaviour in dromedary camels. The results will complement the list of genetic variants previously reported to be associated with morphometric traits in dromedaries [17] afterscreening a larger number of animals and a higher-density SNP array. They will also serve to explore the genomic basis of biomechanical and behavioural traits in this livestock species for the first time. Overall, the insights gained from this research will inform future breeding programs, guide conservation efforts, and enrich our understanding of the genomic features of early domestication and modern selection in camels.

Results and discussion

Altogether, the results from the present study are consistent with the well-documented concept of ‘domestication syndrome’ in mammals. This term refers to a set of morphological, physiological, and behavioral traits that result from genetic changes associated with domestication. Specifically for Old World camels, Fitak, Mohandesan [21] detected recent, positive selection for 107 candidate genes linked to neural crest deficiencies and altered thyroid hormone-based signaling in camel species. Such candidate genes underlie traits collectively recognized within the just-referred ‘domestication syndrome’. Upon examination, we found that none of the candidate genes identified in our study have been reported as genes under positive selection in the dromedary camel populations in existing literature [22,23,24]. Hence, our study contributes novel insights into candidate genes that may be relevant for understanding the effects of domestication and modern selection in dromedaries. Furthermore, the fact that none of our candidate genes have been reported as under positive selection in previous studies highlights the genetic diversity among dromedary camels inhabiting at different locations and suggest that different populations may experience unique selective pressures or adaptations. In turn, we emphasize the importance of examining different camel populations to understand their specific evolutionary trajectories.

Genotypic clustering reflects intergroup differentiation and slight introgression

Principal Component Analysis (PCA) based on 50 K genotypes revealed that raising farm is a significant clustering criterion for study dromedary camels (Fig. 1; PC1 and PC2 explained 16.5% and 8.4% of genetic variation, respectively). For example, farms 2 and 3 are the largest reserves of Canarian dromedaries, and they are genetically connected through the exchange of living animals for breeding purposes. At these farms, dromedaries are sorted into subgroups based on their sex, age, and phenotypic characters. Farm-specific breeding programs might have led to the selection of distinct genetic lines, thereby causing the observed genetic differentiation between animals within Farm 2 and 3. Additionally, environmental factors and selective pressures unique to each farm could also contribute to the genetic divergence observed within these subpopulations. These farms are the primary source for living animals of Farm 1 [25, 26] and the rest of Europe. In contrast, Farm 4’s genetic connection with the others is less frequent, which may explain its relatively unique genetic structure. Such genetic differentiation among Canarian camel’s breeding farms coincide with the results of previous researches aimed at studying phenotypic diversity for camel zoometrics on the same study population [27]. Instead, the factor ‘farm’ did not have a significant discriminatory effect on camel biomechanical and behavioral performance [28, 29]. Camel gait is a highly conserved ancestral trait [30]. Concerning behavior, this trait tends to be evolutionarily conserved across populations [31], especially when environmental conditions and management practices are relatively uniform across farms. Since behavioral traits are often influenced by essential genetic factors mostly linked to survival and adaptation, they can remain stable despite genetic differentiation.

Fig. 1
figure 1

Principal components analysis (PCA) results displaying the clustering of 120 Canarian dromedary camels raised at 4 farms according to their 50 K genotypes

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This clustering patternalso serves to explain the phenotypic diversity encountered in the study sample. Descriptive statistics (minimum (Min), maximum (Max), mean, and standard deviation (SD)) for the 12 phenotypes recorded in 120 dromedary camels are presented in Table 1. High variability, particularly for body morphometrics and Intelligence Quotient, was noted. Both environmental pressures and functional specialization at domestic scenarios significantly influence the morphology and psyche of the animals [32]. However, physical performance traits showed little variation, likely due to the conserved nature of camel trait [30].

Table 1 Descriptive statistics (minimum (Min), maximum (Max), mean, and standard deviation (SD)) for the zoometrics, biomechanics and behaviour traits recorded in 120 dromedary camels
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Overall, the structure of the study animal population suggests that human-driven selection of dromedary camels maintainsassortative mating for size and behavior akin to natural populations [33]. Under the condition of gregarious animal species, assortative mating is crucial for optimizing energy investment towards reproductionand survival in arid environments.

Linkage disequilibrium pattern supports the suitability of the study population and SNP array density for accurate high-resolution genomic mapping

The LD decay plot is shown in Fig. 2. Moderate LD (r2 = 0.20) is present at 100 kb between markers. This finding aligns with the LD patterns described by Bahbahani [34], where similar distances for moderate LD (r2 = 0.25) were observed. Differences in LD patterns may arise from variations in sample size, genomic coverage, and genotyping methods.

Fig. 2
figure 2

Linkage disequilibrium (LD) decay plot depicted from pairwise LD values (r2) against genetic distance (Kb) between genomic markers across dromedary camel genome

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Assuming a size for camel genome of 2.2 Gb, achieving saturation of the genome with an average resolution of 100 kb would necessitate 22,000 fully informative SNPs. It means that a minimum of 22,000 SNPs are required to cover the genome and capture LD information for genome-wide association studies in camels [35]. Our study exceeds this threshold, with 49,632 SNPs retained after quality control, and all 120 animals included in the analysis.

Variations in camel body morphometrics might correlate to increased prevalence and incidence of sensory and cognitive impairments

Seven SNPs at genome-wide level (Fig. 3) and twenty-nine SNPs at chromosome-wide level were significantly associated with zoometrics-related traits in dromedary camels. Twenty-three different candidate genes were identified (Table 2). None of these genes overlap with those reported previously in other studies that investigated the genetic basis of growth and morphometric traits in dromedaries [17, 18, 36]. Although future functional studies will allow for a more precise confirmation of gene functions in dromedaries, we rely on previous association studies in multiple species (mammals and zebrafish), considering that genome-wide association signals are enriched in orthologous genes associated in other species, as suggested by Gualdrón Duarte, Yuan [37].

Fig. 3
figure 3

Manhattan and Q-Q plots displaying the results of the genome-wide association study for zoometrics-related trait ‘Length’ in dromedary camels. Negative log10 P-values (y-axis) of the associations between SNPs and length phenotypes are plotted against the genomic location of each SNP marker (x-axis). Blue line represents the threshold of genome-wide significance after correction for multiple testing (q-value = 0.05)

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Table 2 Genome- and chromosome-wide significant associations between SNP markers and zoometrics-related traits in dromedary camels
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PVRIG, STAG3, GAL3ST4, TRAPPC14, and LAMTOR4 genes affect width and perimeter/girth measurements in dromedary camels. These genes are lassociated with various conditions in humans, mice and zebrafish. They are linked to neurodegenerative and neuropsychiatric processes, which can affect eye size and morphology, cause microcephaly, and lead to abnormal ciliogenesis, cilia instability, reduced thigmotactic behavior, decreasedlocomotor activity, and hyperactivity. They are also related to immune response, including lymphadenomegalia and T-cell function. Regarding reproductive performance, they are associated withinfertility, abnormal embryo size, and embryonic/preweaning lethality. Additionally, these genes are connected to cell cycle regulation and skeletal structure, impacting bone density and rib morphology [38,39,40,41,42,43].

Four (ZCCHC8, RSRC2, KNTC1, and U6) and seven (TENM2, LYN, RPS20, SNORD54, MOS, KCNV2, and PUM3) additional genes regulate width and perimeter/girth measurements, respectively. ZCCHC8, RSRC2, KNTC1, and U6 genes are linked to neoplastic processes, decreased reproductive performance, narrow eye opening, motor neuron diseases, retinitis pigmentosa, poikiloderma with neutropenia, and recessive intellectual disability in humans and mice [38, 44,45,46,47]. Instead, those genes that are specifically associated with perimeter/girth measurements in our study, are widely recognized for their implication on morpho-functional alterations at sensory-neural tissues and organs, neoplastic processes, immune structures, and pigmentation in humans and animal models. Concretely, TENM2, KCNV2, and PUM3 genes are associated with abnormalities at retina ganglion, cone-rod distribution, eye size, visual cortex, superior colliculus, and lateral geniculate nucleus in humans, mice, and zebrafish [48,49,50]. The just-referred structures play essential roles in normal visual processing and orienting motor responses, visuospatial attention, and perceptual decision-making. LYN gene is related to a wide range of neoplastic processes in humans [45] and immune dysfunctions in mice [51, 52]. In addition, abnormal pigmentations at the skin, epidermis, ear, and tail, as well as decreased exploratory behaviour, are phenotypes associated to genomic variability in RPS20 gene in mice [53, 54]. Interestingly, the association of RPS20 gene with perimeter/girth measurements in dromedary camels provides further evidence to support the correlations previously found between body morphometrics (height at withers, chest girth, and hump girth) and weight, leadership behaviour, and coat pigmentation in dromedary camels by Iglesias Pastrana, Navas González [25]. MOS gene, however, has been mostly associated to reduced reproductive performance and cell cycle alterations in mice [55, 56].

Lastly, phenotypic variability for length measurements was found to be controlled by other seven candidate genes (PCDH15, NFASC, SAMD12, SPAG16, POU2F2, ZNF574, and GRIK5). PCDH15, NFASC, SAMD12, POU2F2, and GRIK5 genes are associated with decreased general behaviour activity, quality of musculoskeletal movement and balance (propioception), visual and hearing capacity, and inmmune function, as well as increased prevalence of neurodevelopmental disorders with central and peripheral motor dysfunction (i.e., hemorrhagic brain, abnormal synaptic transmission and postsynaptic currents, syndromic intellectual disability, and increased startle reflex and thermal nociceptive threshold) in humans, mice, rats, and zebrafish [57,58,59,60,61,62,63,64,65]. A missense variant in PCDH15 gene is also responsible for the unexpectedly low number of homozygous haplotype carriers for two different Holstein haplotypes that are related to insemination success and neonatal survival in cattle [66]. On the other hand, SPAG16 gene is linked to decreased reproductive performance [67,68,69] and increased prevalence of ciliary dyskinesia (PCD), a X-linked disorder that mainly affects respiratory tissues [70], in humans, mice, and cattle. ZNF574 gene is a hub gene of adipose tissue metabolism in cattle [71] and tumor regulation in humans [72,73,74].

Developmental dysplasia and heart abnormalities may underlie decreased locomotor performance in dromedary camels

Twenty-four SNPs at the chromosome-wide level of significance were significantly associated with biomechanical traits in dromedary camels (Table 3). Eleven candidate genes, which can play potential roles in camels based on their known functions in other mammalian species/animal models (orthologous genes) [37], were identified. MIR187, FBXO8, and TTC28 genes affect displacement and spatial position measurements. Altered expression of these genes correlates with diverse malignancies and the regulation of inflammation, cell stemness, insulin secretion, and embryonic development in humans and mice [75,76,77]. Furthermore, the downregulation of MIR187 gene is linked to intellectual disability and temporal lobe epilepsy in humans and animal models [78, 79].FBXO8 gene is also involved in motor neuron degeneration in humans [80]. Additionally, TTC28 gene is associated with bone and heart abnormalities in mice [53], and increased feed conservation ratio in pig [81].

Table 3 Genome- and chromosome-wide significant associations between SNP markers and biomechanical traits in dromedary camels
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Acceleration-related traits in dromedaries are controlled by six different genes (PRSS56, CHRND, CHRNG, EIF4E2, EFHD1, and GRID1). Loss of PRSS56 gene function leads to impaired visual acuity in humans and mice [82]. CHRND and CHRNG gene mutations cause congenital myasthenic and multiple pterygium syndrome/fetal akinesia in humans, mice, zebrafish, and dogs [83,84,85,86,87]. Various mutant mice models for EIF4E2 gene served to unraveling the role of this gene in the regulation of synaptic plasticity and autism spectrum disorder-associated behaviors [88]. In addition, Sun, Huang [89] and Sun, Yang [90] founded that this gene was also associated with the response to exercise in buffalo and protects the heart against hypoxia in zebrafish. Similarly, mutant mice and wildtype (AB line) zebrafish were used to unravel the functional role of EFHD1 gene in axonal morphogenesis, cardiac mitoflash activation, protection of cardiomyocytes from ischemia, and brain general development and function [91,92,93]. GRID1 gene variants are linked to schizophrenia, bipolar disorder, intellectual disability, and spastic paraplegia in humans [94, 95]Mice lacking GRID1 gene suffer from sensorineural hearing loss [96].

Lastly, MYLK4 gen controls velocity traits in dromedary camels. MYLK4 gene polymorphisms are related to skeletal muscle metabolism and hypertrophic cardiomyopathy in mice [97, 98]; growth and meat tenderness traits cattle [99, 100], goat [101] and pig [102]; energy metabolism in muscle in Chinese perch [103]; and milk production traits in water buffalo [104].

Embryonic neurogenesis and neurodegeneration could shape the behavioural patterns and processes of dromedary camels

Behavioural traits in dromedaries were associated with nine SNPs at genome-wide level (Fig. 4) and fifty-five SNPs at chromosome-wide level of significance (Table 4). Thirty-eight novel candidate genes were identified. The potential role of these genes in dromedaries is pressumed, until species-specific functional studies do exist, basing on the related information existing for orthologous genes in other multiple species [37].

Fig. 4
figure 4

Manhattan and Q-Q plots displaying the results of the genome-wide association study for behavioural trait ‘Intelligence Quotient’ in dromedary camels. Negative log10 P-values (y-axis) of the associations between SNPs and IQ-related phenotypes are plotted against the genomic location of each SNP marker (x-axis). Blue line represents the threshold of genome-wide significance after correction for multiple testing (q-value = 0.05)

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Table 4 Genome- and chromosome-wide significant associations between SNP markers and behavioural traits in dromedary camels
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CACNA1E gen was found to be associated with both cognition and intelligence-linked traits. Polymorphisms in this gen are linked to impaired glucose metabolism, motor dysfunction, and heightened fear/depression/anxiety-like behaviours in mice and rats [105,106,107]. Eleven other genes (MZT1, BORA, DIS3, PIBF1, KLF5, KLF12, GPC5, ABCC4, ERCC5, DST, and CACNA1E) were associated with intelligence traits. MZT1, BORA, DIS3, PIBF1, and KLF5 are linkedto syndromic intellectual disability and autism spectrum disorder in humans [108]. A homozygous haplotype-related loss-of-function variant has been also identified in bovine DIS3, most likely causing embryonic lethality [109]; and mutations in humans DIS3 engrosses the list of risk factors for multiple myeloma [110]. PIBF1 additionally regulates embryonic development and litter size in mice and sheep [111], and is associated with an increased incidence of alterations in neural tube closure/morphology and Joubert syndrome (varying degrees of physical, mental, and visual impairments) in animal models such as mice and frog [53, 112]. KLF5 and KLF12 mutant and wild-type mice are biased for the prognosis of cardiovascular diseases given their differential inner capabilities of structural remodeling of the heart and blood vessels [113, 114], and the severity of clinical pancreatic cancer [115], respectively. GPC5 and ABCC4 genes mutations have been confirmed to be functionally implicated in skeletal and growth defects, neural tube closure defects, and predisposition to nephrotic syndrome in humans, pigs, frogs and zebrafish [116,117,118,119]. Further shreds of evidence ascertained that non-synonymous mutations in ABCC4 gene ascribe to reproductive traits in cattle, buffalo, and pig [120], and resistance to paratuberculosis in cattle [121]. Heritable disorders resulting from mutations in the ERCC5 gene include both cancer and neurodegenerative processes (intracranial malformations and cerebro-oculo-facio-skeletal syndrome) in humans and mice [122, 123]. DST gene has been also reported to be implicated in hereditary sensory and autonomic neuropathies in humans and mice [124].

Lastly, the Intelligence Quotient was regulated by twenty-seven genes. Such genes play significant roles in the self-renewal, early embryo development, and reprogramming of embryonic stem cells in mice [125], and predisposition to intellectual disability in rats (TEX10) [65]; prevalence and incidence of cardiovascular-renal-hepatic-pancreatic dysplasia in zebrafish, mice and humans (INVS and PTPN18) [53, 126, 127]; human and mice senescence and premature aging, which in turn can be implicated in the development of age-related neurodegenerative processes (UBE2E3) [128]; incidence of recessive ocular coloboma and neural tube defects in humans and mice (SALL2) [129, 130]; olfaction (OR10G2, OR10G3¸OR4E2, and OR4E1) [131] and protection against caries (TRAV4) in humans [132]; increased risk of motor system dysfunctions (i.e., amyotrophic lateral sclerosis and benign hereditary chorea) and several autoimmune diseases in Drosophila, humans and rats (SCFD1) [65, 133, 134]; high prevalence of progressive cochleo-vestibular dysfunction (reduced linear vestibular evoked potential and sensorineural hearing loss) in humans, mice and rats (COCH) [53, 65, 135]; thigmotaxis, hyperactivity, vertical activity, brain-lung-thyroid syndrome, severe intellectual disability, mild fever-sensitive seizure, developmental delay, spastic paraplegia, muscular atrophy, cardiovascular failure, microcephaly, and short stature, in humans and animal models (STRN3, AP4S1, PUS7, ATP2A3, ZZEF1 and PXN) [53, 136,137,138,139,140]; regulation of neuronal differentiation and pathogenesis of Alzheimer disease in humans, mice and zebrafish (ZNF536, U1 and SRPK2) [141,142,143]; muscle function, energy and redox metabolism during exercise in mice (SIRT4) [144]; incidence of diet-induced obesity and risk of diabetes and atherosclerosis in humans and mice (PLA2G1B) [145]; and incidence of abnormalities in neurocranium morphology, size and vascular perfusion in mice and rats (MSI1) [53, 65].

Conclusions

The interindividual phenotypic variability in zoometrics, biomechanics and behaviour-related traits in dromedary camels is controlled by polygenic determinants that are located on multiple chromosomes. A total of 124 SNPs, mapped to 70 different candidate genes involved in synthesizing biological products, have been identified as significantly associated with these functional traits. These genes primarily regulate various neurodevelopmental processes and sensory perception. Our findings enhance the empirical understanding of the genomic features of early domestication and modern selection in dromedary camels, and will inform future sustainable breeding and conservation programs for this species. In particular, the integration of gene function analysis, genomics-based selection and proper sub-grouping of individuals based on phenotypyic similarities (assortative natural behaviour) in human-controlled environments will greatly support efforts to preserve the health and welfare of camels.

Methods

Phenotype assessment and blood sampling

Between October 2019 and July 2020, one hundred twenty Canarian dromedary camels (70 males and 50 females; reared at 4 different semi-extensive farms (2 farms in Canary Islands and 2 farms in mainland Spain)) were phenotyped for body morphometrics, biomechanics, and behaviour related traits. A total of thirty zoometric measurements were taken from each animal as indicated by Iglesias Pastrana, Navas González [146]. Zoometric measurements included linear and tridimensional zoometric traits from head, neck, thorax and dorsum, hump, rump and tail, extremities, and feet. Such measurements were aggregated depending on their geometric nature into four phenotypic categories (length, height, width, and perimeter/girth measurements).

Regarding biomechanical performance traits, curve estimation regression statistics was applied to the individual motion measurements for eleven key kinematic variables at ten different anatomic regions, obtained through video analyses, to calculate the coefficients of the mathematical function that best described locomotor behaviour in dromedary camels (cubic function), as described in Pastrana, González [147]. The anatomic regions evaluated for their biomechanics were the cranial angle of the scapula, midway between acromion and head of the humerus (shoulder joint), olecranon (elbow joint), carpus and fetlock (metacarpophalangeal joint) on the forelimb, the iliac crest, greater trochanter of the femur (hip), stifle (knee) joint, point of the hock (tarsus), and fetlock (metatarsophalangeal joint) on the hindlimb. Kinematic variables recorded include acceleration, horizontal acceleration, horizontal position, horizontal velocity, total distance, total horizontal displacement, total vertical displacement, velocity, vertical acceleration, vertical position, and vertical velocity. Biomechanical performance traits were then sub-grouped in four different phenotypic categories, namely: acceleration, velocity, displacement, and spatial position measurements.

Behavioural traits included four phenotypic categories (copying styles, general cognition, intelligence, and Intelligence Quotient (IQ)). First, ‘copying styles’ category comprised behavioural-type coping strategies (proactivity and reactivity displayed by leisure dromedaries in response to social stressors at man-made environments) [28]. Second, ‘general cognition’ category included traits such as dependence, trainabiliy, cooperation, emotional stability, perseverance, get in/out of stables, and ease at handling, Strongly related, the phenotypic category of ‘intelligence’ is composed by the traits: concentration, curiosity, memory, stubbornness, docility, and alertness constituted. Copying styles, general cognition, and intelligence were evaluated through the application of an operant-conditioning problem-solving test. The last category, namely ‘Intelligence Quotient’ (IQ), is a psychometric construct calculated from the individual performance for the general cognition and intelligence related traits [148].

Immediately after individual phenotyping, a blood sample from each dromedary camel was collected through jugular venipuncture in 2 mL vials containing ethylenediaminetetraacetic acid (EDTA) and stored at -20 °C until genomic DNA extraction tasks. DNA was extracted using the QIAamp® DNA Mini Kit according to the manufacturer’s protocol.

Genotyping and standard SNP genotype quality control

High-throughput, high density SNP genotyping array was used to generate the sequence data was used to generate the sequence data (Axiom Camelids Genotyping Array (Affymetrix, CA, USA)) as per the manufacturer’s instructions. This chip cotainss 62,707 SNPs evenly distributed across the dromedary camel genome. The data related to SNP annotation are included in Supplementary Table S 1. Standard quality control procedures were applied to the SNP genotypes using PLINK v1.9. Markers with a call rate below 0.90, a minor allele frequency (MAF) less than 0.02, a Hardy–Weinberg equilibrium p value less than 0.001, and those mapping to sex chromosomes were excluded from the analysis. Additionally, individuals with a genotype call rate lower than 0.95 were susceptible to being excluded from further analyses. After implementing these quality control measures, a total of 49,632 SNPs and all the animals initially included were retained for subsequent analyses. A principal component analysis (PCA) was run with PLINK v1.9 to explore the genetic population structure.

Linkage disequilibrium

Linkage disequilibrium (LD), the degree of non-random association of alleles between loci or correlation between genotypes of markers, was estimated for each pairwise combination of SNPs using the software PopLDdecay [149]. According to McKay, Schnabel [35], in QTL mapping, r2 is favored as the measure of linkage disequilibrium because it quantifies the degree of information that one locus (which may be a quantitative trait or disease-related and potentially unobservable) can provide about another locus. Consequently, r2 is useful for estimating the number of loci required in association studies.

Genome-wide association study (GWAS) for zoometrics, biomechanics, and behaviour-related traits

Following the methodology of Macri, Luigi-Sierra [150], genotype-phenotype association analysis was conducted using the Genome-wide Efficient Mixed-Model Association (GEMMA) v0.98.1 package [151]. The phenotypic information used was the mean quantitative value per each categorical phenotype described and animal (length, height, width, perimeter/girth, acceleration, velocity, displacement, spatial position, copying styles, general cognition, intelligence, and Intelligence Quotient). For each phenotype, a univariate linear mixed model was fitted according to the following formula:

$$\mathrm y=\mathrm{W\alpha}\;+\;\mathrm{x\beta}\;+\;\mathrm u\;+\;\mathrm\varepsilon;\mathrm u\;\sim\;{\mathrm{MVN}}_{\mathrm n}\;\left(0,\lambda\mathrm\;\mathrm\tau^{-1}\;\mathrm K\right)\;,\;\mathrm{and}\;\mathrm\varepsilon\;\sim{\mathrm{MVN}}_{\mathrm n}\;\left(0,\mathrm\tau^{-1}\;{\mathrm I}_{\mathrm n}\right)$$

where y represents an n-vector of zoometrics-, biomechanics-and behaviour-related phenotypes for n = 120 individuals; W is an n × c matrix (c = number of fixed factors) that includes a column of 1s and the fixed effects, namely, sex (2 levels) and age category (3 levels); α is a c-vector denoting the corresponding fixed effects, including the intercept; x represents a n-vector of marker genotypes; β represents the marker’s effect size (allele substitution effect); u is a n-vector of random individual effects that are normally distributed, u ~ N(0, λ τ−1 K), where τ−1 denotes the residual error variance, λ represents the ratio between the two variance components, and K is a SNP genotypes-derived n × n known relatedness matrix. Lastly, ε represents a n-vector of errors, and In represents an n × n identity matrix; while MVNn depicts the multivariate normal distribution with n dimensions. P-values obtained for each association were adjusted for multiple testing with the False Discovery Rate (FDR) method (q-value). In the context of genome-wide association studies (GWAS), the q-value represents the false discovery rate for a given p-value. It estimates the proportion of false positives among the results with a p-value less than or equal to the q-value. In other words, the q-value helps to control for multiple comparisons and reduces the likelihood of reporting false positives, providing a more accurate measure of statistical significance in large-scale studies. Associations with a p-value and q-value below 0.05 were deemed statistically significant. Manhattan plots were generated using the “qqman” R package. The estimation of the proportion of phenotypic variance that can be explained by a specific SNP (PVE) was performed using the following formula [152]:

$$\mathrm{PVE}=\frac{2\mathrm\beta^2\;\mathrm{MAF}\;\left(1-\mathrm{MAF}\right)}{2\mathrm\beta^2\;\mathrm{MAF}\;\left(1-\mathrm{MAF}\right)\;+\;\left[\mathrm{se}\left(\mathrm\beta\right)\right]^2\;2\mathrm N\;\mathrm{MAF}\;\left(1-\mathrm{MAF}\right)}$$

where β represents the SNP variant estimated effect size, se(β) represents the β estimate standard error, MAF denotes the minor allele SNP frequency, and N is the size of the sample. The P lambda function from the R package QCEWA was used to calculate lambda (λ) inflation factors, and quantile-quantile (Q-Q) plots were generated using the ggqqplot function. The Biomart tool from Ensembl was used to retrieve genes located within a flanking region of ± 50 kb of the significant SNPs [17].

Availability of data and materials

Phenotypes and genotypes of dromedary camels involved in this study are available from the Figshare https://figshare.com/account/login#/projects/212105.

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Acknowledgements

The authors would also like to thank ‘Aires Africanos’ Eco-tourism Company, Oasis Park Fuerteventura, and ‘Camelus’ Camellos de Almería, for their direct technical help and assistance.

Funding

The present research was carried out in the financing framework of the international project CA.RA.VA.N - “Toward a Camel Transnational Value Chain” (Reference APCIN-2016-00011-00-00) and during the covering period of a predoctoral contract (FPU Fellowship) funded by the Spanish Ministry of Science and Innovation and a Ramón y Cajal Post-Doctoral Contract with the reference MCIN/AEI/https://doi.org/10.13039/501100011033 and the European Union “NextGenerationEU”/PRTR.

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Authors and Affiliations

  1. Department of Genetics, Faculty of Veterinary Sciences, University of Córdoba, Córdoba, Spain

    Carlos Iglesias Pastrana, Francisco Javier Navas González, Martina Macri, María del Amparo Martínez Martínez & Juan Vicente Delgado Bermejo

  2. Animal Breeding Consulting S.L, Parque Científico Tecnológico de Córdoba, Córdoba, Spain

    Martina Macri

  3. Department of Biosciences, Biotechnologies and Environment, Faculty of Veterinary Sciences, University of Bari ‘Aldo Moro’, Bari, Italy

    Elena Ciani

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  1. Carlos Iglesias Pastrana
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  2. Francisco Javier Navas González
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  3. Martina Macri
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  4. María del Amparo Martínez Martínez
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  5. Elena Ciani
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  6. Juan Vicente Delgado Bermejo
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Contributions

C.I.P, F.J.N.G., E.C. and J.V.D.B. conceived the project and designed the study. C.I.P., F.J.N.G. and J.V.D.B. carried out the phenotypic data collection. M.M., A.M.M. and E.C. completed the DNA extractions. C.I.P., F.J.N.G., M.M. and A.M.M. conducted the statistical analyses. C.I.P. and F.J.N.G. wrote the manuscript. All authors contributed to the editing and refinement of the final manuscript.

Corresponding author

Correspondence to Carlos Iglesias Pastrana.

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Ethics approval and consent to participate

All methods are reported in accordance with ARRIVE guidelines. Experimental protocols were exempt from approval as credited by The Spanish Ministry of Economy and Competitivity through the Royal Decree Law 53/2013 and its credited entity, the Ethics Committee of Animal Experimentation from the University of Córdoba, permitted the application of the protocols present in this study as cited in the 5th section of its 2nd article, as the animals assessed were used for credited zootechnical use. This national Decree follows the European Union Directive 2010/63/UE, from the 22 September of 2010. All farms included in the study followed specific codes of good practices and therefore, the animals received humane care in compliance with the national guide for the care and use of laboratory and farm animals in research. All owners gave their informed consent for the inclusion of their animals before they participated in the study. The study was conducted in accordance with the Declaration of Helsinki.

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The authors declare no competing interests.

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Iglesias Pastrana, C., Navas González, F.J., Macri, M. et al. Identification of novel genetic loci related to dromedary camel (Camelus dromedarius) morphometrics, biomechanics, and behavior by genome-wide association studies. BMC Vet Res 20, 418 (2024). https://doi.org/10.1186/s12917-024-04263-w

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BMC Veterinary Research

ISSN: 1746-6148

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