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Evolutionary Relationship between the Aardwolf, Cats and Dogs

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Published: 8th Feb 2020 in Biology

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Aardwolves are cats, not dogs.  

 

Introduction

Aardwolf (Prosteles cristatus) is a termite feeding specialist that belong to the Family Hyaenidae (Order Carnivora: suborder Feliformia). In this family are three other extant bone-crushing species of hyenas: spotted hyena (Crocuta Crocuta), brown hyena (Parahyaena brunnea), and striped hyena (Hyaena hyaena)1. Aardwolves have been investigated for its classification several times due to its uncertain place in the phylogeny. They were first grouped with the civets (genus Viverra) as V. cristata by Sparrman, 17832, then reclassified as follows: V. hyenoides by Desmarest, 1820, P. lalandii  by Geoffroy St-Hilaire, 1824, and P. typicus by Smith 1834; all of which are now synonyms of P. cristatus 2.

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The order Carnivora is split into two suborders, Feliformia consisting of ‘cat-like’ carnivorans and Caniformia consisting of ‘dog-like’ carnivorans3. The family Hyaenidae resemble dogs more than cats, however they are currently classed under the suborder Feliformia even though the name ‘aardwolf’ means ‘earth wolf’ in Afrikaans which stems from its dog-like features. Unlike cats, they have non-retractable claws, however, unlike dogs, they have no baculum (penis-bone). And unlike both cats and dogs, aardwolves have greatly reduced premolars and molars, broad and hard palate, large tongue, and sticky saliva due to its specialised diet.

The phylogenetic placement of aardwolf has not been certain in the past (6). Due to their visible canid-like characteristics and their current classification under Feliformia, there is often confusion around whether aardwolf actually belongs in Feliformia, in other words, whether they are more related to ‘cats’ (feliforms) than ‘dogs’ (caniforms). Hence,  the phylogenetic relationship between aardwolf, feliforms, and caniforms were revised here using the cytochrome b (cytb) gene sequences for which data are available for the chosen species for this tree construction. In this report, I propose a phylogenetic hypothesis for aardwolf including 18 extant Carnivoran species. The phylogeny is based on a maximum likelihood analysis of cytb sequences, a marker that has proven reliable for mammals3. In this report, the cytb sequences are used to build a phylogenetic tree in a software called ‘MEGA X’ to determine whether aardwolf is more closely related to ‘cats’ than ‘dogs.’ I hypothesise that the current classification of aardwolf under Feliformia is correct, and that their canid-like features are due to convergent evolution.

Methods

To determine the evolutionary relationship between aardwolf, ‘cats’, and ‘dogs’, a phylogeny of Order Carnivora was constructed focusing on family Hyaenidae, Felidae, and Canidae. For this study, sequences of cytb for each of the species included in this study was used. The cytb sequence for all species considered were 1140 base pairs long. The sequences were obtained from searching the NCBI nucleotide database. Specifications of how and where the samples were sourced are briefed in Table 1. An ingroup from each suborder was chosen, and five species which the cytb sequences were available were chosen from both Felidae and Canidae, and all four species of Hyaenidae. Two outgroups were chosen from the order Cetacea as they are grouped with the species of interest under class Mammalia. Evolutionary analyses were conducted in MEGA X software4. A total of 18 sequences were aligned by ClustalW with both pairwise and multiple alignments with gap opening penalty of 15.00 and gap extension penalty of 6.66. The evolutionary history was inferred by using the maximum likelihood method and the best model chosen, General Time Reversible model5 with rates among sites as discrete Gamma distribution.  The phylogeny was run under consensus of 500 bootstrap replicates6. MEGA-X automatically applies Neighbour-Join and BioNJ algorithms to a matrix of pairwise distances estimated using the Maximum Composite Likelihood (MCL) for the initial tree search. 

MEGA-X v10.0.5 was used for tree searching because it is a well-established method for phylogenetic analyses which other researchers have employed (e.g., [14],  . It has an easy user interface for beginners and many tutorials are available on the web which users can follow when constructing their own phylogenies and testing evolutionary theories. MEGA allows comparative analysis of homologous gene sequences and provides an option to build a tree and its statistical result4. DNA sequences or sequences of many genes are readily available on GenBank via the NCBI nucleotide database. MEGA X also provides the option to save the phylogeny construction history as file formats which can be read on R software, which the user can use for another purpose, such as pruning the tree.

Results

Figure 1. A Bootstrap consensus tree of the phylogeny including the aardwolf, its family, Canidae and Felidae based on maximum likelihood estimates with Cetacea as the outgroup at the bottom. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are shown next to the branches6.

Evolutionary analysis was performed on MEGA-X by Maximum Likelihood method.  A tree with the highest maximum log likelihood was identified with the highest bootstrap value support for most evolutionary relationships. Branches corresponding to partitions reproduced in less than 50% bootstrap replicates are automatically collapsed MEGA, however no branches seemed to have collapsed as all 18 species are present in the tree. The tree is visibly splitting in the two suborders. Each suborder is forming a clade with a high support of 100% bootstrap value from maximum likelihood estimates for feliformia that this organisation is well supported, as well as the organisation of the caniformia clade with 100% bootstrap value. However, the species in family Felidae are multifurcating with a relatively low support for this subclade. The Canidae is multifurcating, but with a 100% support. The outgroup of cetacean species is correctly lying outside these two groups indicating that the outgroup is the most distantly related group to the two suborder clades and this position is also supported by a 100% bootstrap value. Ailurus fulgens is positioned between the two clades with no bootstrap value. Most importantly, species within current caniformia classification are forming a clade as is the species within current feliformia classification. This means that the aardwolf is in a clade with the felid species, an indication that aardwolf is more closely related to cats than dogs.

Discussion

The high bootstrap value of 100% for the position of aardwolf forming a clade with all the feliformian species confirms that aardwolf is more closely related to cats than dogs (Fig. 1). My hypothesis was supported as the produced tree shows that aardwolf is more closely related to cats than dogs genetically, which may indicate that the canid-like features of aardwolves as well as the other members of the Hyaenidae group are probably a result of convergent evolution.

The phylogenetic position of aardwolf has not been certain in the past due to its lack of fossil records and their caniform features as well as some feliform characteristics. There have not been many studies focusing on their relationship between cats and dogs, however studies that has included aardwolf in building phylogenetic trees has revealed them being included in suborder feliformia, same as the founded tree in Figure 1, and alongside Felidae and other feliform sister taxa like Eupleridae3 6 (Fig. 1). With studies that do focus on aardwolf, they usually look at its position within family Hyaenidae to determine whether it is the most basal species of the group and its divergence time1,18.

Studies have highlighted the importance of including molecular data when building phylogenetic relationships and testing evolutionary hypotheses. Morphological data is not very reliable in some species due to convergent evolution. Molecular based phylogenetic analyses are significant and important in species like the aardwolf as morphological based analyses were problematic for aardwolf6. This is because other than many primitive morphological characteristics aardwolves have, they have several uniquely derived morphological characteristics such as their dentition 6.  Due to their highly specialised diet, their dentition is severely reduced, making comparative analyses ineffective when considering aardwolf as a member of Hyaenidae in the past1 6. Fossil records are also very important to include when establishing phylogenetic relationships as it may infer the researcher about the time of divergence from the group and may explain some of the convergence in some of the characteristics, such as the morphological transition that led to the evolution of the aardwolf’s unique ecology and associated craniodental morphology 1.

Phylogeny greatly benefits conservation biology by providing possible extra units (e.g., evolutionary significant unit) and currencies (e.g., phylogenetic distinctiveness). It is therefore vitally important to devise diverse approaches for phylogenetic reconstruction for designing conservation efforts. YU

[25] Ryder OA. Species conservation and systematics: the dilemma

of subspecies. Trends Ecol Evol 1986;1:9 –10.

[26] Purvis A, Gittleman J, Brooks T. Phylogeny and conservation.

New York: Cambridge University Press; 2005.

-          “ant hyena” or civet hyena, based on the habit of secreting substances from its anal gland, a characteristic shared with the African civet.

-          The penis remains inserted for the entire period, but with no copulatory tie as found in canids (Ewer 1973; Richardson 1987b).

Classification

GenBankscientific name

GenBankaccession number

Data source

Cetacea

(Outgroup)

Balaena mysticetus

X75588

Tissue samples obtained from stranded or by-catch animals or from delphinaria (aquarium). DNA was extracted from blood, skin, spleen, or liver tissue from frozen or specimens preserved in dimethyl sulphoxide7,8. Cytb gene was isolated.

Cephalorhynchus hectori 

AF084071

Majority are tissue samples of skin. DNA was extracted, cytb sequence was isolated9.

Carnivora

Caniformia

Family Ailuridae

Ailurus fulgens (Ingroup)

NC_011124

DNA samples gifted from Stephen J. O’Brien, Laboratory of Genome Diversity, National Cancer Institute, USA10. Complete genome was sequenced. Cytb gene sequence was obtained by specifying the region to be viewed on the NCBI site.

Family Canidae

Canis lupus familiaris

KF907307

Source and kind of sample not specified.

Canis latrans

KT447695

Chrysocyon brachyurus

KJ508409

No publication is attached to this accession number.

Nyctereutes procyonoides

MG256392

Unspecified sample from the Animal Farm of Institute of Special Wild Animals and Plants in Jilin Province in Northeast China11. Complete genome was sequenced. Cytb gene sequence was obtained by specifying the region to be viewed on the NCBI site.

Urocyon cinereoargenteus

JF489121

Tissue and blood sample collected in the field. Regions not specified. Cytb gene isolated and sequenced12.

Feliformia

Family Eupleridae

Salanoia concolor

(Ingroup)

AY187007

Skin sample from Field Museum of Natural History, USA. Cytb gene was isolated from DNA extracted from skin sample13.

Family Felidae

Catopuma temminckii

FJ594957

Mitochondrial DNA extracted from fibroblast; source of animal not specified. Cytb gene was isolated and sequenced14.

Acinonyx jubatus

AY463959

Samples of muscle, liver, and blood was obtained from cheetah #2 of EEP population. DNA was isolated15. Complete genome was sequenced. Cytb gene sequence was obtained by specifying the region to be viewed on the NCBI site.

Felis catus

NC_001700

DNA and RNA were extracted from lymphocyte16. Source of animal not specified. Complete genome was sequenced. Cytb gene sequence was obtained by specifying the region to be viewed on the NCBI site.

Lynx rufus

GQ979707

Unpublished article – could not be accessed.

Family Pantherinae

Panthera leo persica

KU234271

Blood sample from male Asiatic lion from Nehru Zoological Park, India. Complete mitochondrial genome was sequenced17.

Family Hyaenidae

Hyaena hyaena

AY928678

Extracted DNA from tissue samples. Cytb gene sequence was obtained by specifying the region to be viewed on the NCBI site1.

Proteles cristatus

AY928679

Crocuta crocuta

AY928676

Parahyaena brunnea

AY928677

Table 1. Specifications of the classification, scientific name, GenBank accession number, and source of sequences of species included in the construction of the phylogeny built in this study.

References

1. Koepfli, K. P. et al. Molecular systematics of the Hyaenidae: Relationships of a relictual lineage resolved by a molecular supermatrix. Mol. Phylogenet. Evol. 38, 603–620 (2006).

6.Westbury, M., Cahsan, B., Dalerum, F., Norén, K. & Hofreiter, M. Aardwolf Population Diversity and Phylogenetic Positioning Inferred Using Complete Mitochondrial Genomes. African Journal of Wildlife Research 49, (2019).

2.        Koehler, C. & Richardson, P. Proteles cristatus. Mammalian Species 1 (1990).    doi:10.2307/3504197

3. Agnarsson, I., Kuntner, M. & May-Collado, L. J. Dogs, cats, and kin: A molecular species-level phylogeny of Carnivora. Mol. Phylogenet. Evol. 54, 726–745 (2010).

4.  Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution 35, 1547-1549 (2018).

5.        Hasegawa, M., Kishino, H. & Yano, T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160-174 (1985).

6.  Felsenstein, J. Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution 39, 783 (1985).

7. Árnason, Ú. & Gullberg, A. Relationship of baleen whales established by cytochrome b  gene sequence comparison. Nature 367, 726-728 (1994).

8. Milinkovitch, M., Orti, G. & Meyer, A. Revised phylogeny of whales suggested by mitochondrial ribosomal DNA sequences. Nature 361, 346-348 (1993).

9. Leduc, R. G., Perrin, W. F. & Dizon, A. E. Phylogenetic relationships among the delphinid cetaceans based on full cytochrome B sequences. Mar. Mammal Sci. 15, 619–648 (1999).

10. Arnason, U., Gullberg, A., Janke, A. & Kullberg, M. Mitogenomic analyses of caniform relationships. Mol. Phylogenet. Evol. 45, 863–874 (2007).

11. Sun, L. W., Yang, Y. & Li, G. Y. The complete mitochondrial genome of the raccoon dogs (Canidae: Nyctereutes ussurienusis) and intraspecific comparison of three Asian raccoon dogs. Mitochondrial DNA Part B Resour. 4, 670–671 (2019).

12. Naidu, A., Fitak, R. R., Munguia-Vega, A. & Culver, M. Novel primers for complete mitochondrial cytochrome b gene sequencing in mammals. Mol. Ecol. Resour. 12, 191–196 (2012).

13. Yoder, A. D. et al. Single origin of Malagasy Carnivora from an African ancestor. Nature 421, 734–737 (2003).

14. Rattanasuk, S. & Ketudat-cairns, M. Genetic Diversity of Felids ’ Cytochrome B. 16, 30000 (2009).

15. Burger, P. A. et al. Analysis of the mitochondrial genome of cheetahs (Acinonyx jubatus) with neurodegenerative disease. Gene 338, 111–119 (2004).

16. Lopez, J. V., Cevario, S. & O’Brien, S. J. Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 33, 229–246 (1996).

17. Tabasum, W., Ara, S., Rai, N., Thangaraj, K. & Gaur, A. Complete mitochondrial genome sequence of asiatic lion (Panthera leo persica). Mitochondrial DNA Part B Resour. 1, 619–620 (2016).

18. Cherin, M., Iurino, D. A., Njau, J. K. & Masao, F. T. Nuovo materiale di ienidi (Mammalia, Carnivora) dalla Gola di Olduvai, Tanzania (Pleistocene Inferiore). Boll. della Soc. Paleontol. Ital. 55, i–ix (2016).

 

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