A genomics approach reveals insights into the importance of gene losses for mammalian adaptations

Abstract

Identifying the genomic changes that underlie phenotypic adaptations is a key challenge in evolutionary biology and genomics. Loss of protein-coding genes is one type of genomic change with the potential to affect phenotypic evolution. Here, we develop a genomics approach to accurately detect gene losses and investigate their importance for adaptive evolution in mammals. We discover a number of gene losses that likely contributed to morphological, physiological, and metabolic adaptations in aquatic and flying mammals. These gene losses shed light on possible molecular and cellular mechanisms that underlie these adaptive phenotypes. In addition, we show that gene loss events that occur as a consequence of relaxed selection following adaptation provide novel insights into species’ biology. Our results suggest that gene loss is an evolutionary mechanism for adaptation that may be more widespread than previously anticipated. Hence, investigating gene losses has great potential to reveal the genomic basis underlying macroevolutionary changes.

Convergent vomeronasal system reduction in mammals coincides with convergent losses of calcium signalling and odorant‐degrading genes

“…To uncover genomic changes that could be associated with the loss of the VNS, we screened the genomes of 106 placental mammalian species for protein‐coding genes that were preferentially inactivated in independent lineages that lost the VNS. To detect convergent gene losses, we used a slightly improved version of a previously established forward genomics approach (Hecker et al, ; Sharma et al, ). We required that a gene is lost in at least three out of the five VNS‐reduced lineages, was lost in at least 50% of the species with a reduced VNS, but not lost in more than 10% of the species with an intact VNS (see Section 2.2 for further details).…”

“…We used a forward genomics approach (Hecker et al, ; Hiller et al, ; Sharma et al, ) to identify genes that were preferentially inactivated in mammals with a reduced VNS, but that are intact in most mammals with a morphologically intact VNS. We grouped species into the five independent lineages that lost an essential component (VNO or AOB or both) of the VNS.…”

“…Recent developments in comparative genomics provide insights into genomic changes that are associated with different environmental adaptations during mammalian evolution. In this context, the inactivation of protein‐coding, also referred to as gene loss, has recently received more and more attention (Albalat & Canestro, ; Sharma et al, ). The inactivation or loss of protein‐coding genes reflects adaptations to diverse ecological niches including the change to a subterranean or aquatic habitat (Chikina, Robinson, & Clark, ; Ehrlich et al, ; Huelsmann et al, ; Kishida, Kubota, Shirayama, & Fukami, ; Lopes‐Marques et al, ; Nery, Arroyo, & Opazo, ; Partha et al, ; Prudent, Parra, Schwede, Roscito, & Hiller, ; Sharma et al, ) and various nutrition strategies that range from carnivory, herbivory, insectivory to frugivory (Hecker, Sharma, & Hiller, ; Huelsmann et al, ; Jiang et al, ; Kim et al, ; Liu et al, ; Lopes‐Marques et al, ; Sharma et al, ).…”

“…However, these studies focused on selected candidate genes and investigated either only a small set of species or a specific clade. To overcome these limitations and to gain a broader understanding into genomic changes associated with VNS reduction, we performed the first systematic screen for convergently inactivated protein‐coding genes associated with the convergent reduction of the VNS using the forward genomics principle (Hecker et al, ; Hiller et al, ; Sharma et al, ). Considering 106 placental mammals, we detected a clear association between the inactivation of Trcp2 and the reduction of the VNS.…”

Gene copy number variations as signatures of adaptive evolution in the parthenogenetic, plant‐parasitic nematode Meloidogyne incognita

“…In line with these observations, the present work, conducted at the whole‐genome scale, revealed an unprecedented level of magnitude of gene copy loss events in virulent genotypes and thus supports the view that gene loss could be a common class of adaptive genetic change in response to the stress generated by host resistance in plant‐parasitic nematodes. Recent studies have highlighted the importance of adaptive gene losses as a prevalent evolutionary force that affects organisms from all life kingdoms and contributes to morphological, physiological and metabolic adaptations to changes in environmental conditions (e.g., Casewell, ; Sharma et al., ). From a mechanistic point of view, the loss of a given gene may result from either the drastic loss of a DNA fragment (e.g., following the mobilization of a transposable element), or the slow, iterative accumulation of mutations leading to a final loss of function (e.g., during pseudogenization).…”