Adaptive Introgression as an Evolutionary Force: A Meta-Analysis of Knowledge Trends

Abstract

There is growing evidence for the role of introgressive hybridization in promoting species adaptation (i.e., adaptive introgression) owing to increasing genomic studies on a diversity of taxa over the past decades. However, introgressive hybridization was, and still is, regarded as a homogenizing process hindering the evolutionary process of adaptation to selection pressures. Despite methodological advances, key gaps remain in understanding how adaptive introgression due to hybridization functions across taxonomic groups and biological levels. This study has three objectives: (1) to explore historical trends in the understanding of adaptive introgression, particularly its genomic and functional dimensions; (2) to investigate structural organismal characteristics influencing patterns of adaptive introgression; and (3) to evaluate how adaptive introgression interacts with counteracting evolutionary mechanisms. We carried out a systematic review of the adaptive introgression literature and a multidimensional meta-analysis. The current knowledge trends have been shaped by the genomic revolution. Since 2012, genomic studies have contributed to establishing a clearer understanding of adaptive introgression. The amount and variety of published studies increased from bacteria to mammals across a complexity gradient, focusing on the genomic level and progressively having consequences at a greater number of levels of biological organization (from physiological and demographic to behavioral/ecological). Testing for tendencies, our study also revealed evolutionary mechanisms linked to adaptive introgression co-occurring with divergence forces, demonstrating that these processes are not mutually exclusive, even when they act in opposite directions, i.e., convergence and divergence, such as autosomal introgression (versus islands of differentiation in sex-linked chromosomes), balancing selection (versus genetic drift), or sexual selection (versus assortative mating). This balance is mediated by environmental conditions as they are frequently reported in the studies, regardless of the organisms' structural complexity, shaping the path of the evolutionary process of introgressing species. Studying introgression patterns has important implications for understanding adaptation in rapidly changing environments.

Keywords: adaptive introgression; biological organization; evolution; meta‐analysis; structural complexity; systematics review; trends in knowledge.

FIGURE 1

Temporal evolution of knowledge trends according to the percentage of papers published per year that provide evidence for specific characteristics of adaptive introgression. Dashed line shows the tipping point representing the beginning of the genomic revolution in adaptive introgression studies.

FIGURE 2

Bipartite network of adaptive introgression's reported characteristics, in different levels of biological organization, and the taxonomic groups, across a taxonomic complexity gradient (node size represents the total number of papers describing each characteristic and the edges' thickness represents standardized edges weights (stEW) of each connection (a). Bar chart showing the effect of the Taxonomic Group factor (A—Prokaryotes, B—Single‐cell eukaryotes, C—Eukaryotes with sex‐linked chromosomes and random mating, and D—Eukaryotes with sexual selection) on the percentage of connections across the levels of biological organization. Bars represent mean values with standard deviation. Significant results from detailed multiple comparisons of means are provided in Table S3 (Supporting Information) (b). Cladogram with the potential evolutionary cleavage moments of adaptive introgression functionality (c). Genomics/cytology's layer (Autosomal introgression [IntrogA], Autosomal islands of differentiation [IslA], Nuclear introgression [IntrogN], Introgression on Sex‐chromosomes [IntrogS], Cytoplasmic introgression [IntrogC], Islands of differentiation in nucleus [IslN], Islands of differentiation on Sex‐chromosomes [IslS], Cytoplasmic islands of differentiation [IslC], and the presence of balancing selection [BalSel]); Physiology's layer (endogenous impacts on adaptive introgression [EndImp], Haldane's rule compliance [HalRule], exception to Haldane's rule [NoHalR], female sterility [FemStl], male sterility [MalStl], any sterility [AnStl], sex‐bias introgression [SexBI], paternal biased‐direction of introgression [PatDir], and maternal biased‐direction of introgression [MatDir]); Demography's layer (demographic disparities [Demogr], any demographic disparities [NoDem], direction of introgression from native to colonizers [NatToC], and exception to native‐to‐colonizers direction [NoNatC]); Behavior's layer (presence of sexual selection [SexSel], presence of assortative mating [Assort], presence of intra‐sexual interspecific competition [SexComp], and absence of intra‐sexual interspecific competition [NoComp]); and Ecology's layer (environmental‐mediated introgression [EnvMed], iteration between allopatric and sympatric periods along evolutionary history [TempCy], exogenous impacts on adaptive introgression [ExImp], allele surfing [AlSurf], and no allele surfing [NoAlSf]).

FIGURE 3

Heatmap of pairwise standardized edges' weight (_stEW) among adaptive introgressions reported characteristics and the taxonomic groups.

FIGURE 4

Eigenvector and PageRank metrics from multilayer network analyses considering both multilayer values (across different levels) and aggregate values (without level consideration). Circles size represents the average of standardized edges weights (stEW) between different adaptive introgression characteristics at inter‐level (left side) and intra‐level (right side).