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The formation of new species via the accumulation of incompatible genetic changes is thought to result either from ecologically based divergent natural selection or the order by which mutations happen to arise, leading to different evolutionary trajectories even under similar selection pressures. There is growing evidence in support of both ecological speciation and mutation-order speciation, but how different environmental scenarios affect the rate of species formation remains underexplored. We use a simple model of optimizing selection on multiple traits (“Fisher’s geometric model”) to determine the conditions that generate genetic incompatibilities in a changing environment. We find that incompatibilities are likely to accumulate in isolated populations adapting to different environments, consistent with ecological speciation. Incompatibilities also arise when isolated populations face a similar novel environment; these cases of mutation-order speciation are particularly likely when the environment changes rapidly and favors the accumulation of large-effect mutations. In addition, we find that homoploid hybrid speciation is likely to occur either when new environments arise in between the parental environments or when parental populations have accumulated large-effect mutations following a period of rapid adaptation. Our results indicate that periods of rapid environmental change are particularly conducive to speciation, especially mutation-order or hybrid speciation.

Geographic isolation is considered essential to most speciation events, but our understanding of what controls the pace and degree of phenotypic divergence among allopatric populations remains poor. Why do some taxa exhibit phenotypic differentiation across barriers to dispersal, whereas others do not? To test factors controlling phenotypic divergence in allopatry, we employed a comparative phylogeographic approach consisting of replicates of ecologically similar Andean bird species isolated across a major biogeographic barrier, the Marañon Valley of Peru. Our study design leverages variation among codistributed taxa in their degree of plumage, morphometric, and vocal differentiation across the Marañon to examine the tempo of phenotypic evolution. We found that substantial plumage difference between populations required roughly two million years to evolve. In contrast, morphometric trait evolution showed greater idiosyncrasy and stasis. Our results demonstrate that despite a large degree of idiosyncrasy in the relationship between genetic and phenotypic divergence across taxa and environments, comparative studies within regions may reveal predictability in the pace of phenotypic divergence. Our results also suggest that social selection is important for driving differentiation of populations found in similar environments.

Divergence with gene flow is well documented and reveals the influence of ecological adaptation on speciation. Yet, it remains intuitive that gene exchange inhibits speciation in many scenarios, particularly among ecologically similar populations. The influence of gene flow on the divergence of populations facing similar selection pressures has received less empirical attention than scenarios where differentiation is coupled with local environmental adaptation. I used a paired study design to test the influence of genomic divergence and introgression on plumage differentiation between ecologically similar allopatric replacements of Andean cloud forest birds. Through analyses of short-read genome-wide sequences from over 160 individuals in 16 codistributed lineages, I found that plumage divergence is associated with deep genetic divergence, implicating a prominent role of geographic isolation in speciation. By contrast, lineages that lack plumage divergence across the same geographic barrier are more recently isolated or exhibit a signature of secondary genetic introgression, indicating a negative relationship between gene flow and divergence in phenotypic traits important to speciation. My results suggest that the evolutionary outcomes of cycles of isolation and divergence in this important theatre of biotic diversification are sensitive to time spent in the absence of gene flow.

Background Reproductive isolation can result from adaptive processes (e.g., ecological speciation and mutation-order speciation) or stochastic processes such as “system drift” model. Ecological speciation predicts barriers to gene flow between populations from different environments, but not among replicate populations from the same environment. In contrast, reproductive isolation among populations independently adapted to the same/similar environment can arise from both mutation-order speciation or system drift. Results In experimentally evolved populations adapting to a hot environment for over 100 generations, we find evidence for pre- and postmating reproductive isolation. On one hand, an altered lipid metabolism and cuticular hydrocarbon composition pointed to possible premating barriers between the ancestral and replicate evolved populations. On the other hand, the pronounced gene expression differences in male reproductive genes may underlie the postmating isolation among replicate evolved populations adapting to the same environment with the same standing genetic variation. Conclusion Our study confirms that replicated evolution experiments provide valuable insights into the mechanisms of speciation. The rapid emergence of the premating reproductive isolation during temperature adaptation showcases incipient ecological speciation. The potential evidence of postmating reproductive isolation among replicates gave rise to two hypotheses: (1) mutation-order speciation through a common selection on early fecundity leading to an inherent inter-locus sexual conflict; (2) system drift with genetic drift along the neutral ridges.

In contrast to ecological speciation, where reproductive isolation evolves as a consequence of divergent natural selection, speciation by parallel natural selection has been less thoroughly studied. To test whether parallel evolution drives speciation, we leveraged the repeated evolution of benthic and limnetic ecotypes of threespine stickleback fish and estimated fitness for pure crosses and within-ecotype hybrids in semi-natural ponds and in laboratory aquaria. In ponds, we detected hybrid breakdown in both ecotypes but this was counterbalanced by heterosis and the strength of post-zygotic isolation was nil. In aquaria, we detected heterosis in limnetic crosses and breakdown in benthic crosses, which is suggestive of process- and ecotype-specific environment-dependence. In ponds, heterosis and breakdown were three times greater in limnetic crosses than in benthic crosses, contrasting the prediction that the fitness consequences of hybridization should be greater in crosses among more derived ecotypes. Consistent with a primary role for stochastic processes, patterns differed among crosses between populations from different lakes. Yet, the observation of qualitatively similar patterns of heterosis and hybrid breakdown for both ecotypes when averaging the lake pairs indicates that the outcome of hybridization is repeatable in a general sense.

There is increasing evidence of segregating sexually antagonistic (SA) genetic variation for fitness in laboratory and wild populations, yet the conditions for the maintenance of such variation can be restrictive. Epistatic interactions between genes can contribute to the maintenance of genetic variance in fitness and we suggest that epistasis between SA genes should be pervasive. Here, we explore its effect on SA genetic variation in fitness using a two locus model with negative epistasis. Our results demonstrate that epistasis often increases the parameter space showing polymorphism for SA loci. This is because selection in one locus is affected by allele frequencies at the other, which can act to balance net selection in males and females. Increased linkage between SA loci had more marginal effects. We also show that under some conditions, large portions of the parameter space evolve to a state where male benefit alleles are fixed at one locus and female benefit alleles at the other. This novel effect of epistasis on SA loci, which we term the ‘equity effect’, may have important effects on population differentiation and may contribute to speciation. More generally, these results support the suggestion that epistasis contributes to population divergence.

Since Darwin published the \"Origin,\" great progress has been made in our understanding of speciation mechanisms. The early investigations by Mayr and Dobzhansky linked Darwin's view of speciation by adaptive divergence to the evolution of reproductive isolation, and thus provided a framework for studying the origin of species. However, major controversies and questions remain, including: When is speciation nonecological? Under what conditions does geographic isolation constitute a reproductive isolating barrier? and How do we estimate the \"importance\" of different isolating barriers? Here, we address these questions, providing historical background and offering some new perspectives. A topic of great recent interest is the role of ecology in speciation. \"Ecological speciation\" is defined as the case in which divergent selection leads to reproductive isolation, with speciation under uniform selection, polyploid speciation, and speciation by genetic drift defined as \"nonecological.\" We review these proposed cases of nonecological speciation and conclude that speciation by uniform selection and polyploidy normally involve ecological processes. Furthermore, because selection can impart reproductive isolation both directly through traits under selection and indirectly through pleiotropy and linkage, it is much more effective in producing isolation than genetic drift. We thus argue that natural selection is a ubiquitous part of speciation, and given the many ways in which stochastic and deterministic factors may interact during divergence, we question whether the ecological speciation concept is useful. We also suggest that geographic isolation caused by adaptation to different habitats plays a major, and largely neglected, role in speciation. We thus provide a framework for incorporating geographic isolation into the biological species concept (BSC) by separating ecological from historical processes that govern species distributions, allowing for an estimate of geographic isolation based upon genetic differences between taxa. Finally, we suggest that the individual and relative contributions of all potential barriers be estimated for species pairs that have recently achieved species status under the criteria of the BSC. Only in this way will it be possible to distinguish those barriers that have actually contributed to speciation from those that have accumulated after speciation is complete. We conclude that ecological adaptation is the major driver of reproductive isolation, and that the term \"biology of speciation,\" as proposed by Mayr, remains an accurate and useful characterization of the diversity of speciation mechanisms.

Abundant evidence supports a role for sexual selection in the evolution of reproductive isolation, and it is thus unsurprising that much attention has been given, both conceptually and empirically, to understanding its role in speciation. In doing so, debate has arisen on how sexual selection fits within the much used ecological versus mutation-order classification of speciation mechanisms, with sexual selection often presented as a distinct third alternative. We argue that models of speciation by sexual selection include a fundamental role of divergent selection between environments or mutation order in initiating the process. Rather than representing a unique mechanism, sexual selection layers a coevolutionary process between males and females on top of the classic mechanisms such that the evolution of each sex can now be driven by divergent selection, mutation order, and selection arising from interactions with the other sex. In addition to blurring the distinction between ecological and mutation-order speciation, this coevolutionary process is likely to speed divergence. Sexual selection is not unique in this way; coevolutionary processes can similarly arise from ecological interactions between populations or species, with similar results. Ultimately, understanding the contribution of sexual selection to speciation will require identifying the processes that drive the divergence of mating biases.

Background Divergent genetic responses to the same environmental pressures may lead sympatric ecological speciation possible. Such speciation process possibly explains rapid sympatric speciation of island species. Two island endemic ginger species Zingiber kawagoii and Z. shuanglongensis was suggested to be independently originated from inland ancestors, but their island endemism and similar morphologies and habitats lead another hypothesis of in situ ecological speciation. For understanding when and how these two species diverged, intraspecific variation was estimated from three chloroplast DNA fragments (cpDNA) and interspecific genome-wide SNPs and expression differences after saline treatment were examined by transcriptomic analyses. Results Extremely low intraspecific genetic variation was estimated by cpDNA sequences in both species: nucleotide diversity π = 0.00002 in Z. kawagoii and no nucleotide substitution but only indels found in Z. shuanglongensis . Nonsignificant inter-population genetic differentiation suggests homogenized genetic variation within species. Based on 53,683 SNPs from 13,842 polymorphic transcripts, in which 10,693 SNPs are fixed between species, Z. kawagoii and Z. shuanglongensis were estimated to be diverged since 218~ 238 thousand generations ago (complete divergence since 41.5~ 43.5 thousand generations ago). This time is more recent than the time of Taiwan Island formation. In addition, high proportion of differential expression genes (DEGs) is non-polymorphic or non-positively selected, suggesting key roles of plastic genetic divergence in broaden the selectability in incipient speciation. While some positive selected DEGs were mainly the biotic and abiotic stress-resistance genes, emphasizing the importance of adaptive divergence of stress-related genes in sympatric ecological speciation. Furthermore, the higher proportional expression of functional classes in Z. kawagoii than in Z. shuanglongensis explains the more widespread distribution of Z. kawagoii in Taiwan. Conclusions Our results contradict the previous hypothesis of independent origination of these two island endemic ginger species from SE China and SW China. Adaptive divergent responses to the stress explain how these gingers maintain genetic differentiation in sympatry. However, the recent speciation and rapid expansion make extremely low intraspecific genetic variation in these two species. This study arise a more probable speciation hypothesis of sympatric speciation within an island via the mutation-order mechanism underlying the same environmental pressure.

Speciation research focuses on the evolutionary mechanisms responsible for the origin of species, and recent treatments have distinguished ecological and mutation-order speciation as distinct evolutionary processes. Using a research framework that considers ‘speciation phenotypes’ (sensu Shaw and Mullen in Genet 139(5):649–661, 2011 ) and a modified hierarchy of speciation models, we address whether speciation in benthic fishes commonly called darters proceeds under divergent ecological selection or a mutation-order process. We examined neutral genetic divergence, sexual signal (male color) divergence, environmental differences, and geographic distance in 66 species pair comparisons. Modified Mantel tests detected significant relationships between genetic distance and overall male color differences, as well as geographic distance and overall male color differences; however, after accounting for the correlation of male color and geographic distance with genetic distance using a partial Mantel test, no relationship was observed between male color and geographic distance. Neither microhabitat nor climatic measures of environmental differences correlated with overall male color differences. Color difference scores for discrete color categories (i.e., red/orange/yellow, black, and blue/green) differed in their correlations with explanatory variables, implying different selection regimes may be influencing each component of darter color patterns. Our results do not support a primary role for divergent ecological selection shaping early divergence of darter sexual signals. Instead, a model of mutation-order speciation may best explain the clock-like manner of changes in male color among darter species.