Molecular mechanisms of adaptation and speciation: why do we need an integrative approach?

Abstract

Understanding divergent adaptation and ecological speciation requires the synthesis of multiple approaches, including phenotypic characterization, genetics and genomics, realistic assessment of fitness and population genetic modelling. Current research in this field often approaches this problem from one of two directions: either a mechanistic approach-seeking to link phenotype, genotype and fitness, or a genomic approach-searching for signatures of divergence or selection across the genome. In most cases, these two approaches are not synthesized, and as a result, our understanding is incomplete. We argue that research in adaptation and evolutionary genetics needs to integrate these approaches for multiple reasons, including progress towards understanding the architecture and evolutionary history of adaptation and speciation loci, the ability to untangle linkage and pleiotropy, increased knowledge of mechanisms of genomic evolution and insights into parallel evolutionary events. Identifying the genetic underpinnings of adaptation and ecological speciation is not necessarily the end goal of research, but it is an integral part of understanding the evolutionary process. As a result, it is critical to utilize both genetic and genomic approaches. Challenges remain, particularly in nonmodel organisms and in our ability to synthesize results from multiple experimental systems. Nonetheless, advances in genetic and genomic techniques are increasingly available in a diverse array of systems, and the time is ripe to exploit the synthesis of these two approaches to increase our understanding of evolution.

Understanding the molecular basis of adaptation to freshwater environments by prawns in the genus Macrobrachium

“…This is because mitochondrial genes are efficient at mining evolutionary ancestral relationships among species, but consequently they provide little or no insight into historical or current adaptive processes (James et al, 2016;Byers et al, 2017).…”

“…It is also conceivable that adaptation and phenotypic convergence can be the result of whole genomic response (Wray, 2013). Because the mitochondrial genome represents only a tiny fraction of the total genome and selection pressures may not act strongly on this small genome, variation in mtDNA genes are unlikely to provide useful information about adaptive processes (Byers et al, 2017). This in part is why mtDNA is considered to essentially evolve in a neutral fashion.…”

“…There is also the possibility that the same genes and mutations are used to address similar problems in closely related populations or taxa (Conte et al, 2012;Byers et al, 2017). Lynch and Conery (2003) and Blank et al (2014) suggested that genome architecture can be shaped by natural selection; any excess DNA that appears in the genome can persist in populations, and can then serve as the basis for adaptations to newly invaded habitats.…”

“…While genomic regions under selection provide efficient adaptations that may have been either retained after isolation or evolved in parallel following colonization of new environments (Hohenlohe et al, 2010;Byers et al, 2017). Due to high abundance, high mutation rate and a maternal inheritance pattern, mtDNA has been the dominant marker(s) used widely in phylogenetic studies; but it can provide little insight into adaptive history (Pyron, 2015;James et al, 2016).…”

“…Due to high abundance, high mutation rate and a maternal inheritance pattern, mtDNA has been the dominant marker(s) used widely in phylogenetic studies; but it can provide little insight into adaptive history (Pyron, 2015;James et al, 2016). It is also highly unlikely that only a few genes or even a small genomic region can provide complete adaptation to a novel environment, rather it is more likely that contributions from many genes or whole genomic response is required for efficient adaptation (Wray, 2013;Byers et al, 2017).…”