How the Galapagos cormorant lost its ability to fly

Introduction

Novel traits play a key role in evolution by facilitating the access to new ecological niches. Novelty is often recognized at a phenotypic level and usually related to gain of new function. But can nature innovate through the loss of the function? Wing reduction and loss of flight in birds occurred several times in evolutionary history. It is found among 26 families of birds. However, it is difficult to determine genetic basis underlying this change.

In this interesting study Burga et al. are using flightless Galapagos cormorant (Phalacrocorax harrisi) as an interesting model to study evolution of recent loss of flight. Namely, P.harrisi diverged from its flighted relatives within the past 2 million years and represents the only flightless cormorant among 40 existing species. The entire population (approximately 1500 individuals) is distributed along the coastlines of Isabela and Fernandina islands in the Galapagos archipelago.

There are two evolutionary paths that could possibly explain the loss of flight. Flightlessness could be positively selected if it helps birds to develop alternative ability to escape from predators and to survive (like swimming). Alternatively, if flying was not essential for surviving (no need to escape from predators) the mutations that obstruct flight might accumulate in the gene pool. These two scenarios are not necessarily mutually exclusive, meaning that passive loss of flight might be followed by positive selection that will keep reducing wings.

Results

In this study authors showed that comparative genomics is a powerful tool for disentangling evolutionary history and for understanding molecular mechanisms behind evolutionary changes. They sequenced, and de novo assembled the complete genomes of the Galapagos flightless cormorant and three flighted relatives.

Initially authors identified highly conserved regions of non-coding DNA in attempt to find potential candidates of the wing shortening but eventually they focused their attention on coding variants. Among coding variants, many genes were identified exclusively in the Galapagos cormorant genome. Variants related with dysfunction of the primary cilium (key role in mediating hedgehog signaling pathway during development) were selected as candidates linked to reduction of the wings. Interestingly, impaired function of the same genes in humans lead to bone development disorders described as skeletal ciliopathies.

To confirm hypotheses about effects of mutations in cilia-related genes, authors combine in vivo experiments in C. elegans and in vitro experiments in mouse chondrogenic cell lines. Experiments in C. elegans confirmed that a missense variant present in Galapagos cormorant IFT122 protein is sufficient to affect cilia function in vivo. Nevertheless, it would be interesting to see if knock-in of some other functional gene from Galapagos cormorant would lead to same behavior as wild type gene from C. elegans (used as positive control in this experiment).

Further analyses were focused on gene called CUX1. This gene is linked to shortened wings in chickens. Results from these experiments suggest that cilia and hedgehog signaling pathway related genes are likely transcriptional targets of CUX1 in chondrocytes. In normal functioning of hedgehog signaling pathway, CUX1 regulates expression of cilia related genes and promotes chondrogenesis. Since Galapagos cormorants carry different variant of the CUX1 gene, this possibly modify gene’s function, influencing both cilia formation and their functioning. All this reflects on hedgehog pathway activity, resulting in impaired bone growth.

Conclusion

This exhaustive study underlined importance of sophisticated genetic tools such as genomic analyses in explaining molecular mechanisms responsible for the changes observable at phenotypic level. Experiments revealed polygenic basis of the flightlessness. Even more, they select ciliary disfunction as a likely contributor to the evolution of loss of flight. Most valuable aspect of this study is its approach that can be used for identification of the other variants responsible for evolutionary innovation by analyzing genomes of closely related species.

 

Burga et al. (2017) A genetic signature of the evolution of loss of flight in the Galapagos cormorant. Science 356 (6341), eaal3345.

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