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Ecological basis and genetic architecture of crypsis polymorphism in the desert clicker grasshopper (Ligurotettix coquilletti)

Timothy K. O’Connor, Marissa C. Sandoval, Jiarui Wang, Jacob C. Hans, Risa Takenaka, Myron Child VI, Noah K. Whiteman

Posted on: 27 May 2021 , updated on: 1 June 2021

Preprint posted on 30 April 2021

Article now published in Evolution at http://dx.doi.org/10.1111/evo.14321

Hiding in plain sight: Crypsis polymorphism in desert clicker grasshoppers is maintained by balancing selection driven by predation pressure, and genetically regulated by structural variants associated with colour morphs

Selected by Riddhi Deshmukh

Background:

Colour polymorphisms are fascinating adaptations that help organisms avoid predation (1–3), gain access to mates (4), and thermoregulate (5,6). Cryptic colouration or camouflage can help organisms blend into their backgrounds. Further, some species exhibit discrete camouflaging morphs in a crypsis polymorphism. Complex adaptations such as colour polymorphisms are often maintained by balancing selection through various processes including negative frequency dependence (7), where rarer forms are advantageous; and sexual antagonism (8), where a trait differentially benefits the two sexes. The individual morph phenotypes can be inherited across generations as a single (9) or multi-locus (10) trait. At the genetic level, these could be governed by individual SNPs (11), differential cis-regulation of certain genes (12), transposable element insertion (13) and structural variation such as large-scale inversions (14) and indels (15). These mechanisms can give rise to alternate alleles that regulate the various morphs.

 

Fig. 1B from the preprint depicting the two cryptic morphs of desert clicker grasshoppers

 

Grasshoppers and other Orthoperans show a notable degree of colour polymorphism, particularly crypsis. The desert clicker (Ligurotettix coquilletti), found across the arid region of Sonoran, Mojave, and Peninsular Deserts in Western USA, shows two cryptic morphs in both sexes. These comprise a uniform morph that has more or less homogeneous patterning, and a banded morph that shows contrasting light and dark bands across the body axis. These grasshoppers spend most of their lifetimes in creosote bushes, however, adult females oviposit on the desert floor, which makes them susceptible to attack from predators. In the preprint, the authors collected desert clickers from 20 sites across the species range, and estimated morph frequencies and their dependence on predation environment (bushes vs desert substrate). They identified dominance relationships between morphs and identified the processes that maintain these morphs across different populations. They also explored the genetic bases of this polymorphism with a novel approach using RADseq to detect structural variants associated with each morph.

 

Key findings:

  1. The authors found that both colour morphs of grasshoppers occurred at intermediate frequencies across different populations. However, these frequencies were unrelated to variation in the host plant stems where they spent most of their lives. Instead, the desert substrate, where females oviposit their eggs, explained most of the variation in morph frequencies. Therefore, predation pressure on ovipositing females was a better indicator of the geographical variation in crypsis polymorphism in desert clicker.
  2. The existence of colour morphs at intermediate frequencies across populations points towards balancing selection as a maintenance mechanism. This could be acting in two possible ways; the frequency of banded morphs and their resemblance to the substrate indicates the presence of negative frequency dependent selection acting on the morphs. However, only females were exposed to predation on the ground during oviposition on the desert floor, suggests the presence of sexually antagonistic selection as well.
  3. The authors used reduced representation RADcap sequencing with bait capture to detect structural variants in the genome associated with the cryptic morphs. They designed sequence capture baits targeting 40,000 loci, and tailored the analysis of the data to grasshopper genomes that have an XX/XO sex-determination mechanism. This novel method provided a cost-effective way to sequence large grasshopper genomes (~6-16 Gb) in the absence of reliable genome assemblies and re-sequencing data.
  4. The authors identified a putative indel that was associated with the colour morphs. The insertion was associated with the banded morph, suggesting that this genomic region may contain loci that regulate patterning and colouration observed in this morph. This result is similar to that found in Timema stick insects, where a 5Mb deletion in the genome disrupts continuous colour variation in this group and results in a discrete polymorphism with green and brown morphs. 
    Fig. 6D-E from the preprint showing association of the indel loci with the banded morph and differences between populations where the banded morph is dominant versus recessive. When the banded morph is recessive, the associated loci would be present in heterozygous uniform individuals as well, causing a shift in the trend of association.

     

  5. The authors found that the dominance relationships between the banded and uniform morphs differed between populations. While the banded form was dominant over much of the range, in a few isolated populations, it was recessive and weakly penetrant. The authors speculate that the banded phenotype may have been ancestrally recessive, but may have subsequently evolved dominance and higher penetrance in certain parts of the species range. This result provides insights into the long-debated question of whether dominance evolves.

 

Why is this work important?

  1. The authors developed a cost-effective approach to sequence large genomes with reduced representation RADseq and used it to ask questions about the genetic bases of adaptations in this system. This method can be applies to any species with discrete morphs. It is an excellent alternative, especially for non-model systems, when genomic data is unavailable, and is a nifty tool to initiate studies on genetic bases of polymorphisms or alternative reproductive strategies.
  2. The authors provide preliminary evidence for the evolution of dominance between morphs in this polymorphic species. Whether dominance arises with individual mutations, or evolves consequentially, has been a fundamental question in an enduring debate in the field. Some aspects of this question can be answered by experimental evolution studies, however, they may not reflect what happens in nature. Studies on wild populations in their native habitat better represent the standing genetic variation that could be used to trace the evolutionary history of morphs.

 

Future directions:

  1. Identifying and characterizing the genomic location of the putative indel, the genes that regulate this crypsis polymorphism, and exploring their evolutionary origin. A second Ligurotettix species also shows colour polymorphism resembling the desert clicker. Do these species share a common genetic bases and mechanisms of maintenance of the polymorphism?
  2. Characterizing the evolution of dominance between morphs. Could allelic turnover have resulted in the evolution of dominance in the banded morph? Or did dominance evolve as a pleiotropic outcome of the indel polymorphism and the selection it imposed on other loci?
  3. How do the inheritance patterns of colour morphs vary when morphs from two populations with different dominance relationships interbreed?
  4. How does the efficiency and accuracy of the RADseq and bait capture approach compare to conventional methods used for such analyses?
  5. What modes of balancing selection are involved in maintaining morph frequencies? Is it possible to determine the contribution from negative frequency dependent selection versus sexually antagonistic selection in maintenance of intermediate morph frequencies across populations and dominance relationships?

 

References:

  1. Symula, R., Schulte, R. & Summers, K. Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry hypothesis. R. Soc. London. Ser. B Biol. Sci. 268, 2415–2421 (2001).
  2. Bond, A. B. The evolution of color polymorphism: crypticity, searching images, and apostatic selection. Rev. Ecol. Evol. Syst. 38, 489–514 (2007).
  3. Quicke, D. L. J. Mimicry, Crypsis, Masquerade and Other Adaptive Resemblances. (Wiley Blackwell, 2017).
  4. Chamberlain, N. L., Hill, R. I., Kapan, D. D., Gilbert, L. E. & Kronforst, M. R. Polymorphic butterfly reveals the missing link in ecological Science (80-. ). 326, 847–850 (2009).
  5. Williams, The distribution of bumblebee colour patterns worldwide: Possible significance for thermoregulation, crypsis, and warning mimicry. Biol. J. Linn. Soc. 92, 97–118 (2007).
  6. Gautam, S. & Kunte, K. Adaptive plasticity in wing melanisation of a montane butterfly across a Himalayan elevational gradient. Entomol. een.12911 (2020) doi:10.1111/een.12911.
  7. Takahashi, Y., Yoshimura, J., Morita, S. & Watanabe, M. Negative frequency-dependent selection in female color polymorphism of a Evolution (N. Y). 64, 3620–3628 (2010).
  8. Kunte, Female-limited mimetic polymorphism: A review of theories and a critique of sexual selection as balancing selection. Anim. Behav. 78, 1029–1036 (2009).
  9. Clarke, A. & Sheppard, P. M. The genetics of the mimetic butterfly Papilio polytes L. Philos. Trans. R. Soc. B 263, 431–458 (1972).
  10. Kronforst, M. R. & Papa, R. The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry. Genetics 200, 1–19 (2015).
  11. Cooke, T. F. et al. Genetic mapping and biochemical basis of yellow feather pigmentation in budgerigars. Cell 171, 427–439.e21 (2017).
  12. Gautier, M. et al. The genomic basis of color pattern polymorphism in the Harlequin Ladybird. Curr. Biol. 28, 3296–3302.e7 (2018).
  13. van’t Hof, A. E. et al. The industrial melanism mutation in British peppered moths is a transposable element. Nature 534, 102–105 (2016).
  14. Joron, M. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011).
  15. Villoutreix, R. et al. Large-scale mutation in the evolution of a gene complex for cryptic coloration. Science (80-. ). 369, 460–466 (2020).

 

 

doi: https://doi.org/10.1242/prelights.29111

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