Genetic diversity, phylogenetic position, and co-phylogenetic relationships of Karyolysus, a common blood parasite of lizards in the Western Mediterranean

The genus Karyolysus Labbé, 1894 was originally proposed to accommodate blood parasites of lacertid lizards in Western Europe. However, recent phylogenetic analyses suggested an inconclusive taxonomic position of these parasites of the order Adeleorina based on the available genetic information. Inconsistencies between molecular phylogeny, morphology, and/or life cycles can reflect lack of enough genetic information of the target group. We therefore surveyed 28 localities and collected blood samples from 828 lizards of 23 species including lacertids, skinks, and geckoes in the Western Mediterranean, North Africa, and Macaronesia, where species of Karyolysus and other adeleorine parasites have been described. We combined molecular and microscopic methods to analyze the samples, including those from the host type species and the type locality of Karyolysus bicapsulatus. The phylogenetic relationship of these parasites was analyzed based on the 18S rRNA gene and the co-phylogenetic relationship with their vertebrate hosts was reconstructed. We molecularly detected adeleorine parasites in 37.9% of the blood samples and found 22 new parasite haplotypes. A phylogenetic reconstruction with 132 sequences indicated that 20 of the newly detected haplotypes clustered in a well-supported clade with another 18 sequences that included Karyolysus galloti and Karyolysus lacazei. Morphological evidence also supported that Karyolysus bicapsulatus clustered in this monophyletic clade. These results supported the taxonomic validity of the genus. In addition, we found some parasite haplotypes that infected different lizard host genera with ancient diverging histories, which suggested that Karyolysus is less host-specific than other blood parasites of lizards in the region. A co-phylogenetic analysis supported this interpretation because no significant co-speciation signal was evidenced between Karyolysus and lizard hosts.Karyolysus属（Karyolysus Labbé, 1894）最初被建立，用以囊括西欧地区蜥蜴科蜥蜴的血液寄生生物。然而，基于现有遗传信息开展的近期系统发育分析显示，这类阿德雷亚目（Adeleorina）寄生生物的分类地位仍不明确。分子系统发育、形态学及/或生活史之间的不一致，可能反映出目标类群遗传信息储备不足。为此，我们在西地中海、北非及马卡罗尼西亚（该区域已报道过Karyolysus属及其他阿德雷亚目寄生生物物种）调查了28个采样点，从23种蜥蜴（涵盖蜥蜴科、石龙子科与壁虎科）的828只个体中采集了血液样本。我们结合分子与显微观测方法对样本展开分析，其中包括取自双囊Karyolysus（Karyolysus bicapsulatus）宿主模式种及其模式产地的样本。我们基于18S核糖体RNA（18S rRNA）基因分析了这类寄生生物的系统发育关系，并重建了其与脊椎动物宿主的共系统发育关系。我们在37.9%的血液样本中通过分子手段检测到阿德雷亚目寄生生物，共发现22个全新的寄生生物单倍型。基于132条序列开展的系统发育重建结果显示，新检测到的20个单倍型与另外18条序列（包含加氏Karyolysus（Karyolysus galloti）和拉氏Karyolysus（Karyolysus lacazei））聚为一个支持度较高的演化支。形态学证据同样证实双囊Karyolysus隶属于该单系演化支，上述结果支持了该属的分类学有效性。此外，我们发现部分寄生生物单倍型可感染具有古老分化历史的不同蜥蜴宿主属，这表明Karyolysus属相较于该区域其他蜥蜴血液寄生生物的宿主特异性更低。共系统发育分析也验证了这一结论，因为未检测到Karyolysus属与其蜥蜴宿主之间存在显著的共物种形成信号。