Howler monkeys ( Alouatta ), comprising between nine and 14 species and ranging from southern Mexico to northern Argentina, are the most widely distributed platyrrhines. Previous phylogenetic studies of howlers have used chromosomal and morphological characters and a limited number of molecular markers; however, branching patterns conflict between studies or remain unresolved. We performed a new phylogenetic analysis of Alouatta using both concatenated and coalescent-based species tree approaches based on 14 unlinked non-coding intergenic nuclear regions. Our taxon sampling included five of the seven South American species ( Alouatta caraya , Alouatta belzebul , Alouatta guariba , Alouatta seniculus , Alouatta sara ) and the two recognized species from Mesoamerica ( Alouatta pigra , Alouatta palliata ). Similarly to previous studies, our phylogenies supported a Mesoamerican clade and a South American clade. For the South American howlers, both methods recovered the Atlantic Forest endemic A. guariba as sister to all remaining South American species, albeit with moderate support. Moreover, we found no support for the previously proposed sister relationship between A. guariba and A. belzebul . For the first time, a clade composed of A. sara and A. caraya was identified. The relationships among the other South American howlers, however, were not fully supported . Our estimates for divergence times within Alouatta are generally older compared to estimates in earlier studies. However, they conform to recent studies proposing a Miocene age for the Isthmus of Panama and for the uplift of the northern Andes. Our results also point to an early genetic isolation of A. guariba in the Atlantic Forest, in agreement with the hypothesis of biotic exchange across South American rain forests in the Miocene. Collectively, these findings contribute to a better understanding of the diversification processes among howler monkey species; however, they also suggest that further comprehension of the evolutionary history of the Alouatta radiation will rely on broadened taxonomic, geographic, and genomic sampling.

中文翻译：

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吼猴辐射的分子系统发育推断（灵长类动物：Alouatta）

吼猴 (Alouatta) 包括 9 到 14 个物种，范围从墨西哥南部到阿根廷北部，是分布最广泛的桔梗。先前对吼叫的系统发育研究使用了染色体和形态特征以及数量有限的分子标记；然而，研究之间的分支模式冲突或仍未解决。我们使用基于 14 个未链接的非编码基因间核区域的串联和基于聚结的物种树方法对 Alouatta 进行了新的系统发育分析。我们的分类群抽样包括七个南美物种中的五个（Alouatta caraya、Alouatta belzebul、Alouatta guariba、Alouatta seniculus、Alouatta sara）和来自中美洲的两个公认物种（Alouattapigra、Alouatta palliata）。与以往的研究类似，我们的系统发育支持中美洲进化枝和南美洲进化枝。对于南美吼叫，这两种方法都将大西洋森林特有的 A. guariba 恢复为所有剩余南美物种的姐妹，尽管得到了适度的支持。此外，我们发现没有支持先前提出的 A. guariba 和 A. belzebul 之间的姐妹关系。首次确定了由 A. sara 和 A. caraya 组成的进化枝。然而，其他南美咆哮者之间的关系并未得到完全支持。与早期研究中的估计值相比，我们对 Alouatta 内发散时间的估计值通常更早。然而，它们符合最近提出的巴拿马地峡和安第斯山脉北部隆起处于中新世时代的研究。我们的结果还表明 A 的早期遗传分离。guariba 在大西洋森林中，与中新世南美雨林生物交换的假设一致。总的来说，这些发现有助于更好地了解吼猴物种的多样化过程；然而，他们还表明，对阿卢阿塔辐射进化历史的进一步理解将依赖于更广泛的分类、地理和基因组抽样。