A transposable element insertion is the switch between alternative life history strategies

Abstract

Correspondence to: AW alyssa.woronik@zoologi.su.se and CWW chris.wheat@zoologi.su.se 20 21 Tradeoffs affect resource allocation during development and result in fitness consequences that 22 drive the evolution of life history strategies. Yet despite their importance, we know little about 23 the mechanisms underlying life history tradeoffs in wild populations. Many species of Colias 24 butterflies exhibit an alternative life history strategy (ALHS) where females divert resources from 25 wing pigment synthesis to reproductive and somatic development. Due to this reallocation, a 26 wing color polymorphism is associated with the ALHS: individuals have either yellow/orange or 27 white wings. Here we map the genetic basis of the ALHS switch in Colias crocea to a 28 transposable element insertion downstream of the Colias homolog of BarH-1, a homeobox 29 transcription factor. Using CRISPR/Cas9 gene editing, antibody staining, and electron 30 microscopy we find morph-specific specific expression of BarH-1 suppresses the formation of 31 pigment granules in wing scales. Lipid and transcriptome analyses reveal physiological 32 differences associated with the ALHS. These findings characterize a novel mechanism for a 33 female-limited ALHS and show that the switch arises via recruitment of a transcription factor 34 previously known for its function in cell fate determination in pigment cells of the retina. 35 36A life-history strategy is a complex pattern of co-evolved life history traits (e.g. number of 37 offspring, size of offspring, and lifespan 1 ), that is fundamentally shaped by tradeoffs that arise 38 because all fitness components cannot simultaneously be maximized. Therefore, finite 39 resources are competitively allocated to one life history trait versus another within a single 40 individual, and selection acts on these allocation patterns to optimize fitness 2 . Evolutionary 41 theory predicts that positive selection will remove variation from natural populations, as 42 genotypes with the highest fitness go to fixation 3 . However, across diverse taxa alternative life 43 history strategies (ALHSs) are maintained within populations at intermediate frequencies due to 44 balancing selection 4 . Life history theory was developed using methods such as quantitative 45 genetics, artificial selection, demography, and modeling to gain significant insights into the 46 causes and consequences of genetic and environmental variation on life history traits. Yet 47 despite these advances, a key challenge that remains is to identify the proximate mechanisms 48 underlying tradeoffs, especially for ecologically relevant tradeoffs that occur in natural 49 populations 5 . Here, we identify the mechanism underlying one such ALHS in the butterfly Colias 50

Dissection of Larval and Pupal Wings of Bicyclus anynana Butterflies

“…Labs around the world have worked with different species to address a variety of questions at the intersection of these fields. Examples include the discovery of the involvement of the gene optix in wing pattern mimicry of Heliconius butterflies [1,2]; discovery of doublesex as a mimicry supergene in Papilio polytes [3]; involvement of Wnt signaling in wing pattern of butterflies such as Junonia coenia, Heliconius erato and Vanesssa cardui [4-6]; involvement of the genes spalt and BarH-1 in the wing pigmentation of multiple Pieris and Colias species [7][8][9]; and the involvement of calcium signaling in wing patterning in Junonia orithya [10] to mention a few.…”