Parallel Independent Losses of G-Type Lysozyme Genes in Hairless Aquatic Mammals

Abstract

Lysozyme enzymes provide classic examples of molecular adaptation and parallel evolution, however, nearly all insights to date come from c-type lysozymes. G-type lysozymes occur in diverse vertebrates, with multiple independent duplications reported. Most mammals possess two g-type lysozyme genes (Lyg1 and Lyg2), the result of an early duplication, although some lineages are known to have subsequently lost one copy. Here we examine g-type lysozyme evolution across > 250 mammals, and reveal widespread losses of either Lyg1 or Lyg2 in several divergent taxa across the mammal tree of life. At the same time, we report strong evidence of extensive losses of both gene copies in cetaceans and sirenians, with an additional putative case of parallel loss in the tarsier. To validate these findings, we inspected published short-read data and confirmed the presence of loss of function mutations. Despite these losses, comparisons of selection pressures between intact g- and c-type lysozyme genes showed stronger purifying selection in the former, indicative of conserved function. Although the reasons for the evolutionary loss of g-type lysozymes in fully aquatic mammals is not known, we suggest that this is likely to at least partially relate to their hairlessness. Indeed, while Lyg1 does not show tissue-specific expression, recent studies have linked Lyg2 expression to anagen hair follicle development and hair loss. Such a role for g-type lysozyme would explain why the Lyg2 gene became obsolete when these taxa lost their body hair.

Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder afrotheria

“…This thyroid hormone synthesis-associated protein also has unique residues in sirenians. Many of the same genes of the integumentary system, particularly those expressed in the outer layers of the skin 32 , 81 – 87 , were lost by both sirenians and cetaceans. Our data support the idea that convergent gene loss occurs in species with similar ecological pressures 88 (here, the transition to a fully aquatic lifestyle by distantly related species over ~50–60 My of evolution).…”

Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder Afrotheria

“…Because the ancestors of extant manatees and the dugong diverged at crown Sirenia ∼30 Mya 2 , these gene changes were likely critical for the transition to an aquatic habitat. Many of the same genes of the integumentary system, particularly expressed in the outer layers of the skin 51,79,114–119 , were lost by both sirenians and cetaceans. This further supports the idea that convergent gene loss occurs in species with similar ecological pressures 120 (here, the transition to a fully aquatic lifestyle by distantly related species over ∼50-60 My of evolution).…”

Molecular Mechanisms Underlying Vertebrate Adaptive Evolution: A Systematic Review

“…MMP12 is involved in extracellular matrix breakdown, and its loss impacts pulmonary elasticity in a way that allows marine mammals to renew ~90% of their air in a single breath, an advantageous trait for diving [47]. The loss of the aforementioned epidermal and hair developmental genes resulted in modifications of the respective developmental pathways, yielding alternative traits of a thicker epidermis and hair loss traits in cetaceans and sirenians, suggested to be advantageous for the aquatic environments [47][48][49].…”