Shou-Hsien Li

Conspicuous colorations are widespread in animals, yet their adaptive functions remain unclear, particularly in mammals. White eye-rings (WER), the bright-colored pelage encircling eyes, are prevalent in rodents (Mammalia: Rodentia). Here we show that WER has repeatedly emerged with transitions to diurnalism and disappeared with reversions to nocturnalism during rodent evolution. In addition, our behavioral tests on the Nile rat (Arvicanthis niloticus, diurnal with WER) and the house mouse (Mus musculus, nocturnal without WER) discover that WER enhances visual appeal (the ability to attract attention or preference) possibly by accentuating facial bilateral symmetry. This effect is neither associated with sexual selection nor species recognition and was absent in house mice. Thus, WER appears to function through sensory exploitation and selectively favored in diurnal rodents capable of perceiving and responding to it, but is constrained in nocturnal species. These findings illustrate how ecological factors and shared sensory preferences shape conspicuous color patterns.

Conspicuous colorations are widespread in animals, yet their adaptive functions remain unclear, particularly in mammals. White eye-rings (WER), the bright-colored pelage encircling eyes, are prevalence in rodents (Mammalia: Rodentia). Phylogenetic analyses across 601 rodents show that WER has repeatedly emerged with transitions to diurnalism and disappeared with reversions to nocturnalism during rodent evolution. To explore WER’s function, we performed behavioral tests on the Nile rat ( Arvicanthis niloticus , diurnal with WER) and the house mouse ( Mus musculus , nocturnal without WER), and found that WER enhances visual appeal (the ability to attract attention or preference), likely by accentuating facial bilateral symmetry. This effect is neither associated with sexual selection nor species recognition and was absent in mice. Thus, WER appears selectively favored in diurnal rodents capable of perceiving and responding to it, but is constrained in nocturnal species. These findings illustrate how ecological factors and shared sensory preferences shape conspicuous color patterns.

Populations of Eurasian otters Lutra lutra, one of the most widely distributed apex predators in Eurasia, have been depleted mainly since the 1950s. However, a lack of information about their genomic diversity and how they are organized geographically in East Asia severely impedes our ability to monitor and conserve them in particular management units. Here, we re‐sequenced and analyzed 20 otter genomes spanning continental East Asia, including a population at Kinmen, a small island off the Fujian coast, China. The otters form three genetic clusters (one of L. l. lutra in the north and two of L. l. chinensis in the south), which have diverged in the Holocene. These three clusters should be recognized as three conservation management units to monitor and manage independently. The heterozygosity of the East Asian otters is as low as that of the threatened carnivores sequenced. Historical effective population size trajectories inferred from genomic variations suggest that their low genomic diversity could be partially attributed to changes in the climate since the mid‐Pleistocene and anthropogenic intervention since the Holocene. However, no evidence of genetic erosion, mutation load, or high level of inbreeding was detected in the presumably isolated Kinmen Island population. Any future in situ conservation efforts should consider this information for the conservation management units.

Significance: A reduction in heterozygosity may limit the opportunity for species facing the same selective pressures to evolve parallel adaptation. Examining 19 East Asian tits’ genomes, we find a pattern of lower heterozygosity in western endemics compared with that found in both eastern endemics and widespread taxa, consistent with expectations of demographic contraction driven by late-Pleistocene climate fluctuations. Comparisons among both endemic and widespread tits find disproportionate levels of genetic differentiation between pairs of lowland and highland tits in genomic regions that are enriched for genes that may be associated with the oxygen transport cascade and/or thermogenesis. However, evolution did not occur in the same genes, and populations with higher heterozygosity did not show higher levels of parallel evolution as predicted.

The long‐term persistence of a population which has suffered a bottleneck partly depends on how historical demographic dynamics impacted its genetic diversity and the accumulation of deleterious mutations. Here we provide genomic evidence for the genetic effect of a recent population bottleneck in the endangered black‐faced spoonbill (Platalea minor) after its rapid population recovery. Our data suggest that the bird's effective population size, N_e, had been relatively stable (7500–9000) since 22,000 years ago; however, a recent brief yet severe bottleneck (N_e = 20) which we here estimated to occur around the 1940s wiped out >99% of its historical N_e in roughly three generations. Despite a >15‐fold population recovery since 1988, we found that black‐faced spoonbill population has higher levels of inbreeding (7.4 times more runs of homozygosity) than its sister species, the royal spoonbill (P. regia), which is not thought to have undergone a marked population contraction. Although the two spoonbills have similar levels of genome‐wide genetic diversity, our results suggest that selection on more genes was relaxed in the black‐faced spoonbill; moreover individual black‐faced spoonbills carry more putatively deleterious mutations (Grantham's score > 50), and may therefore express more deleterious phenotypic effects than royal spoonbills. Here we demonstrate the value of using genomic indices to monitor levels of genetic erosion, inbreeding and mutation load in species with conservation concerns. To mitigate the prolonged negative genetic effect of a population bottleneck, we recommend that all possible measures should be employed to maintain population growth of a threatened species.

Ecogeographic rules that describe quantitative relationships between morphologies and climate might help us predict how morphometrics of animals was shaped by local temperature or humidity. Although the ecogeographic rules had been widely tested in animals of Europe and North America, they had not been fully validated for species in regions that are less studied. Here, we investigate the morphometric variation of a widely distributed East Asian passerine, the vinous‐throated parrotbill (Sinosuthora webbiana), to test whether its morphological variation conforms to the prediction of Bergmann's rule, Allen's rules, and Gloger's rule. We at first described the climatic niche ofS. webbianafrom occurrence records (n = 7838) and specimen records (n = 290). The results of analysis of covariance (ANCOVA) suggested that the plumage coloration of these parrotbills was darker in wetter/warmer environments following Gloger's rule. However, their appendage size (culmen length, beak volume, tarsi length) was larger in colder environments, the opposite of the predictions of Allen's rule. Similarly, their body size (wing length) was larger in warmer environments, the opposite of the predictions of Bergmann's rule. Such disconformity to both Bergmann's rule and Allen's rule suggests that the evolution of morphological variations is likely governed by multiple selection forces rather than dominated by thermoregulation. Our results suggest that these ecogeographic rules should be validated prior to forecasting biological responses to climate change especially for species in less‐studied regions.

What kind of genetic variation contributes the most to adaptation is a fundamental question in evolutionary biology. By resequencing genomes of 80 individuals, we inferred the origin of genomic variants associated with a complex adaptive syndrome involving multiple quantitative traits, namely, adaptation between high and low altitudes, in the vinous-throated parrotbill ( Sinosuthora webbiana ) in Taiwan. By comparing these variants with those in the Asian mainland population, we revealed standing variation in 24 noncoding genomic regions to be the predominant genetic source of adaptation. Parrotbills at both high and low altitudes exhibited signatures of recent selection, suggesting that not only the front but also the trailing edges of postglacial expanding populations could be subjected to environmental stresses. This study verifies and quantifies the importance of standing variation in adaptation in a cohort of genes, illustrating that the evolutionary potential of a population depends significantly on its preexisting genetic diversity. These findings provide important context for understanding adaptation and conservation of species in the Anthropocene.

The glacial-interglacial cycles in the Pleistocene caused repeated range expansion and contraction of species in several regions in the world. However, it remains uncertain whether such climate oscillations had similar impact on East Asian biota, despite its widely recognized importance in global biodiversity. Here we use both molecular and ecological niche profiles on 11 East Asian avian species with various elevational ranges to reveal their response to the late Pleistocene climate changes. The ecological niche models (ENM) consistently showed that these avian species might substantially contract their ranges to the south during the Last Interglacial period (LIG) and expanded their northern range margins through the Last Glacial Maximum (LGM), leading to the LGM ranges observed for all 11 species. Consistently, coalescent simulations based on 25–30 nuclear genes retrieved signatures of significant population growth through the last glacial period across all species studied. Climate statistics suggested that high climatic variability during the LIG and a relatively mild climate at the LGM potentially explained the historical population dynamics of these birds. This is the first study based on multiple species and both lines of ecological niche profiles and genetic data to characterize the unique response of East Asian biota to late Pleistocene climate. The present study highlights regional differences in the evolutionary consequence of climate change during the last glacial cycle and implies that global warming might pose a great risk to species in this region given potentially higher climatic variation in the future analogous to that during the LIG.