Natural phenotypic radiations, with their high diversity and convergence, are well-suited for informing how genomic changes translate to natural phenotypic variation. New genomic tools enable discovery in such traditionally nonmodel systems. Here, we characterize the genomic basis of color pattern variation in bumble bees (Hymenoptera, Apidae, Bombus), a group that has undergone extensive convergence of setal color patterns as a result of Müllerian mimicry. In western North America, multiple species converge on local mimicry patterns through parallel shifts of midabdominal segments from red to black. Using genome-wide association, we establish that a cis-regulatory locus between the abdominal fate-determining Hox genes, abd-A and Abd-B, controls the red–black color switch in a western species, Bombus melanopygus. Gene expression analysis reveals distinct shifts in Abd-B aligned with the duration of setal pigmentation at the pupal–adult transition. This results in atypical anterior Abd-B expression, a late developmental homeotic shift. Changing expression of Hox genes can have widespread effects, given their important role across segmental phenotypes; however, the late timing reduces this pleiotropy, making Hox genes suitable targets. Analysis of this locus across mimics and relatives reveals that other species follow independent genetic routes to obtain the same phenotypes.
Phenotypic polymorphism can constitute an inherent challenge for species delimitation. This issue is exemplified in bumble bees (Bombus), where species can exhibit high colour variation across their range, but otherwise exhibit little morphological variation to distinguish them from close relatives. We examine the species status of one of the most abundant North American bumble bees, Bombus bifarius Cresson, which historically comprised two major taxa, bifarius s.s. and nearcticus. These lineages are recognized primarily by red and black variation in their mid-abdominal coloration; however, a continuum from black (nearcticus) to red (bifarius s.s.) variation has led to their historic synonymization. Integrating mitochondrial and nuclear data and whole-genome sequencing, we reveal a high level of both mitochondrial and nuclear divergence delimiting two morphologically cryptic species -the red bifarius s.s. and the colour-variable (black to red) nearcticus. Population genomic analysis supports an absence of recent genomic admixture and a strong population structure between the two clades, even in sympatry. Species distribution models predict partially differentiated niches between the genetically inferred clades with annual precipitation being a leading differentiating variable. The bifarius s.s. lineage also occupies significantly higher elevations, with regions of sympatry being among the highest elevations in nearcticus. Our data also support a subspecies-level divergence between the broadly distributed nearcticus and the island population vancouverensis. In this paper, we formally recognize the two species, Bombus bifarius Cresson and Bombus vancouverensis Cresson, the latter including the subspecies B. vancouverensis vancouverensis comb.n. and B. vancouverensis nearcticus comb.n., with vancouverensis the name bearer due to year priority.
Müllerian mimicry theory states that frequency-dependent selection should favour geographical convergence of harmful species onto a shared colour pattern. As such, mimetic patterns are commonly circumscribed into discrete mimicry complexes, each containing a predominant phenotype. Outside a few examples in butterflies, the location of transition zones between mimicry complexes and the factors driving mimicry zones has rarely been examined. To infer the patterns and processes of Müllerian mimicry, we integrate large-scale data on the geographical distribution of colour patterns of social bumblebees across the contiguous United States and use these to quantify colour pattern mimicry using an innovative, unsupervised machine-learning approach based on computer vision. Our data suggest that bumblebees exhibit geographically clustered, but sometimes imperfect colour patterns, and that mimicry patterns gradually transition spatially rather than exhibit discrete boundaries. Additionally, examination of colour pattern transition zones of three comimicking, polymorphic species, where active selection is driving phenotype frequencies, revealed that their transition zones differ in location within a broad region of poor mimicry. Potential factors influencing mimicry transition zone dynamics are discussed.
A wide range of research relies upon the accurate and repeatable measurement of the degree to which organisms resemble one another. Here, we present an unsupervised workflow for analyzing the relationships between organismal color patterns. This workflow utilizes several recent advancements in deep learning based computer vision techniques to calculate perceptual distance. We validate this approach using previously published datasets surrounding diverse applications of color pattern analysis including mimicry, population differentiation, heritability, and development. We demonstrate that our approach is able to reproduce the biologically relevant color pattern relationships originally reported in these studies. Importantly, these results are achieved without any task-specific training. In many cases, we were able to reproduce findings directly from original photographs or plates with minimum standardization, avoiding the need for intermediate representations such as a cartoonized images or trait matrices. We then present two artificial datasets designed to highlight how this approach handles aspects of color patterns, such as changes in pattern location and the perception of color contrast. These results suggest that this approach will generalize well to support the study of a wide range of biological processes in a diverse set of taxa while also accommodating a variety of data formats, preprocessing techniques, and study designs.
We revise the species of Conostigmus Dahlbom, 1858 (Hymenoptera: Ceraphronoidea: Megaspilidae) found in North America, north of Mexico. We describe the following 12 new species: Conostigmus dessarti Trietsch & Mikó sp. nov.; C. duncani Trietsch sp. nov.; C. franzinii Trietsch & Mikó sp. nov.; C. johnsoni Trietsch & Mikó sp. nov.; C. lepus Trietsch sp. nov.; C. longiharpes Trietsch sp. nov.; C. michaeli Trietsch sp. nov.; C. minimus Trietsch & Mikó sp. nov.; C. muratorei Trietsch sp. nov.; C. musettiae Trietsch & Mikó sp. nov.; C. rosemaryae Trietsch sp. nov.; and C. washburni Trietsch sp. nov. We also redescribe the following 12 species: Conostigmus abdominalis (Boheman, 1832); C. bipunctatus Kieffer, 1907; C. dimidiatus (Thomson, 1858); C. erythrothorax (Ashmead, 1893); C. laeviceps (Ashmead, 1893); C. muesebecki Dessart & Masner, 1965; C. nigrorufus Dessart, 1997; C. obscurus (Thomson, 1858); C. orcasensis (Brues, 1909); C. pulchellus Whittaker, 1930; C. quadratogenalis Dessart & Cooper, 1975; and C. triangularis (Thomson, 1858). We report specimens of C. abdominalis (Boheman, 1832) and C. bipunctatus Kieffer, 1907 from the Nearctic for the first time, expanding the range from Palearctic to Holarctic for both species. We regard the following 19 species as having uncertain status due to reasons such as missing type specimens: Conostigmus ambiguus (Ashmead, 1893); C. bacilliger (Kieffer, 1906); C. bakeri Kieffer, 1908; C. californicus (Ashmead, 1893); C. canadensis (Ashmead,1888); C. crawfordi (Mann, 1920); C. harringtoni (Ashmead, 1888); C. hyalinipennis (Ashmead, 1887); C. inermis (Kieffer, 1906); C. integriceps (Kieffer, 1906); C. marylandicus (Ashmead, 1893); C. nevadensis (Kieffer, 1906); C. nigripes (Kieffer, 1906); C. ottawensis (Ashmead, 1888); C. pergandei (Ashmead, 1893); C. popenoei (Ashmead, 1893); C. rufoniger (Provancher, 1888); C. schwarzi (Ashmead, 1893); and C. trapezoidus Kieffer, 1908. We transfer Conostigmus arietinus (Provancher, 1887) to Dendrocerus Ratzeburg, 1852, and consider Conostigmus subinermis (Kieffer, 1907) to be absent from the Nearctic and limited to the Palearctic. The Nearctic species C. timberlakei Kamal, 1926 remains incertae sedis. We provide the name Conostigmus fulgidus Mikό and Trietsch to replace the junior homonym Conostigmus lucidus Mikό and Trietsch 2016. We provide a key for the identification of Nearctic Conostigmus species, and provide comments on their natural history. Finally, we infer evolutionary relationships within Megaspilinae using male genitalia and other morphological characters. This work represents the first in-depth study and revision of Conostigmus in North America, and contributes the first annotated identification key to Nearctic Conostigmus species.
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