Adaptation to a pelagic lifestyle in Procellariiformes
Our selection inference uncovered 20 genes evolving under positive
selection in Procellariiformes, being therefore candidates to be
actively involved in the adaptation of the order to a pelagic lifestyle.
Indeed, the GO’s Enrichment analysis of these genes reveals biological
processes related to striated muscle cell differentiation, response to
starvation, and nutrient reservoir activity, that may be related to the
high energy expenditure during the vast distances they cover in the open
ocean, while visual related genes could be related with underwater
vision to fish and night vision (Hayes, Martin, & Brooke, 1991; Martin
& De, 1991; Mitkus, Nevitt, Danielsen, & Kelber, 2016). Positive
selection of genes related to natriuresis also makes sense for
Procellariiformes since this biological process plays a key role to
maintain the osmotic equilibrium in a sodium-rich environment like the
ocean (Gutiérrez, 2014; “Water and Salt Balance in Seabirds,” 2001),
which Procellariiformes perform thanks to the development of salt glands
(modified nasal glands engaged in secretion of salts). Olfactory
receptors, also found here among enriched GOs of positively selected
genes, showed signature of adaptive evolution in shearwaters (C. Silva
et al., 2020), and are crucial to Procellariiformes for navigation
(Gagliardo et al., 2013; Padget, Dell’Ariccia, Gagliardo,
González-Solís, & Guilford, 2017; Pollonara et al., 2015), partner
recognition and mating (Bonadonna & Nevitt, 2004; Hoover et al., 2018;
Strandh et al., 2012), finding their own burrows (Bonadonna &
Bretagnolle, 2002) or foraging (Bastos et al., 2020; Nevitt, 2008;
Nevitt, Veit, & Kareiva, 1995; Yung, Sin, Cloutier, Nevitt, & Edwards,
2019).
We also inferred genes with intensified natural selection in
Procellariiformes, for which the GOs annotations (Table S8) are similar
and coherent to those in the candidate set of genes with positive
selection in all tubenoses, or, in other words, related to the
adaptation of the order to a pelagic lifestyle. For example, molecular
functions such as sensory perception of sound, smell and chemical
stimulus, neurological system process, camera-type eye development are
related with oceanic navigation. On the other hand, functions such as
homeostatic process, renal system, renal response, chloride transport
and regulation of ion transport point to the need of maintaining osmotic
equilibrium. We also found intensified natural selection in genes
participating in functions related to immune response (like inflammatory
response, defense response, response to wounding, wound healing,
positive regulation of phagocytosis, etc.), accompanied by a relaxation
of natural selection in regulators of blood constituents, induction of
bacterial agglutination, regulation of antigen processing and
presentation, viral budding via host ESCRT complex or macrophage antigen
processing and presentation. As Procellariiformes exposure to parasites
is high (Khan et al., 2019) and their life-history traits favour
parasite maintenance within populations (McCoy et al., 2016), the tuning
between the intensification and relaxation of natural selection in
multiple biological processes and molecular functions related with
immune response would have emerged following an arms race-like model.
For example, as many parasites of tubenoses are blood-feeding, the
intensified natural selection on the thrombin-activated receptor
signaling pathway (GO:0070493), may be an evolutionary response to
counter the anticoagulant activity that most blood-feeding parasites
present (Bensaoud et al., 2018).
Among the gene families expanded in the branch of Procellariiformes, the
one encoding olfactory receptors is remarkable as it is coherent not
only with the finding of a gene with positive selection in all
Procellariiformes with the same functional annotation (g16276.t1 in theP. mauretanicus reference annotation, Table 4) but also with 3
olfactory receptors genes with intensification selection in the same
branch (g14377.t1, g16276.t1 and g17936.t1 in P. mauretanicusreference annotation, Table S8). This triple evidence highlights the
importance of how the adaptation to a pelagic life resulted in the
enhancement of the olfactory function in Procellariiformes, as we
discussed already in the paragraphs above. Moreover, Silva et al. 2020
obtained similar results of positive selection in olfactory genes inC. borealis . Physiologically, tubenoses have one of the largest
olfactory bulb to brain size (OB) ratio of all birds (Cobb, 1968)