Population genomics and sexual signals identify reproductive interference in Uperoleia

When closely related species come into contact via range expansion, both may experience reduced fitness as a result of the interaction. Selection is expected to favor traits that minimize costly interspecies reproductive interactions (such as mismating) via a phenomenon called reproductive character displacement (RCD). Research on RCD frequently assumes secondary contact between species, but the geographic history of species interactions is often unknown. Landscape genomic data allows tests of geographic hypotheses about species origins and secondary contact through range expansion. We used landscape genomic data from single nucleotide polymorphisms (SNPs), mitochondrial sequence data, advertisement call data, and morphological data to investigate a species complex of toadlets (Uperoleia borealis, U. crassa, U. inundata) from northern Australia. Although the three species of frogs were morphologically indistinguishable in our analysis, we determined that U. crassa and U. inundata form a single species (synonymized here) based on an absence of genomic divergence. SNP data identified the phylogeographic origin of U. crassa as the Top End, with subsequent westward invasion into the range of U. borealis in the Kimberley. We identified six F1 hybrids, all of which had the U. borealis mitochondrial haplotype, suggesting unidirectional hybridization. Consistent with the RCD hypothesis, U. borealis and U. crassa sexual signals differ more in sympatry than in allopatry. Hybrid males have intermediate calls, which likely reduces attractiveness to females. Integrating landscape genomic data, mitochondrial sequencing, morphology, and behavioral approaches supplies us an unusually detailed collection of evidence for reproductive character displacement following range expansion and secondary contact.

当近缘物种通过范围扩张发生接触时，二者均可能因种间互作而出现适合度（fitness）下降。自然选择将青睐于通过生殖性状置换（reproductive character displacement, RCD）这一机制，演化出能够降低代价高昂的种间生殖互作（如错配交配）的性状。尽管有关RCD的研究通常默认物种间存在二次接触，但物种互作的地理历史往往难以探明。景观基因组数据（landscape genomic data）可用于检验关于物种起源及通过范围扩张实现二次接触的地理假说。
本研究利用基于单核苷酸多态性（single nucleotide polymorphisms, SNPs）的景观基因组数据、线粒体序列数据、广告鸣唱数据以及形态学数据，对澳大利亚北部的短头蟾属（Uperoleia）物种复合群（包含U. borealis、U. crassa、U. inundata三个类群）展开研究。尽管本研究中三个类群在形态学上无法区分，但基于基因组无显著分化的结果，我们将U. crassa与U. inundata合并为同一物种（本文中将二者作为同物异名处理）。单核苷酸多态性数据显示，U. crassa的系统地理起源为Top End，随后其向西扩散至金伯利地区的U. borealis分布范围中。我们共鉴定出6个F1杂交子代（F1 hybrid），所有个体均携带U. borealis的线粒体单倍型，提示存在单向杂交事件。符合RCD假说的预期，U. borealis与U. crassa的性信号在同域分布（sympatry）区的差异显著大于异域分布（allopatry）区。杂交雄性个体的鸣唱声处于中间表型，这可能会降低其对雌性的吸引力。本研究整合景观基因组数据、线粒体测序、形态学数据与行为学研究方法，为范围扩张与二次接触后的生殖性状置换现象提供了极为详实的证据。