scholarly journals Mitochondria and the Origin of Species: Bridging Genetic and Ecological Perspectives on Speciation Processes

2019 ◽  
Vol 59 (4) ◽  
pp. 900-911 ◽  
Author(s):  
M Tobler ◽  
N Barts ◽  
R Greenway
Keyword(s):  
Reproductive Isolation ◽  
Mitochondrial Function ◽  
Biological Diversity ◽  
Adaptive Divergence ◽  
Hybrid Fitness ◽  
Prezygotic Isolation ◽  
Future Studies ◽  
Natural Systems ◽  
Natural And Sexual Selection ◽  
Mitochondrial Adaptation

Abstract Mitochondria have been known to be involved in speciation through the generation of Dobzhansky–Muller incompatibilities, where functionally neutral co-evolution between mitochondrial and nuclear genomes can cause dysfunction when alleles are recombined in hybrids. We propose that adaptive mitochondrial divergence between populations can not only produce intrinsic (Dobzhansky–Muller) incompatibilities, but could also contribute to reproductive isolation through natural and sexual selection against migrants, post-mating prezygotic isolation, as well as by causing extrinsic reductions in hybrid fitness. We describe how these reproductive isolating barriers can potentially arise through adaptive divergence of mitochondrial function in the absence of mito-nuclear coevolution, a departure from more established views. While a role for mitochondria in the speciation process appears promising, we also highlight critical gaps of knowledge: (1) many systems with a potential for mitochondrially-mediated reproductive isolation lack crucial evidence directly linking reproductive isolation and mitochondrial function; (2) it often remains to be seen if mitochondrial barriers are a driver or a consequence of reproductive isolation; (3) the presence of substantial gene flow in the presence of mito-nuclear incompatibilities raises questions whether such incompatibilities are strong enough to drive speciation to completion; and (4) it remains to be tested how mitochondrial effects on reproductive isolation compare when multiple mechanisms of reproductive isolation coincide. We hope this perspective and the proposed research plans help to inform future studies of mitochondrial adaptation in a manner that links genotypic changes to phenotypic adaptations, fitness, and reproductive isolation in natural systems, helping to clarify the importance of mitochondria in the formation and maintenance of biological diversity.

scholarly journals Ecological divergence in sympatry causes gene misregulation in hybrids

2019 ◽  
Author(s):  
Joseph A. McGirr ◽  
Christopher H. Martin
Keyword(s):  
Gene Expression ◽  
Reproductive Isolation ◽  
Differentially Expressed ◽  
F1 Hybrids ◽  
Adaptive Divergence ◽  
Lower Hybrid ◽  
Hybrid Fitness ◽  
Hybrid Gene ◽  
San Salvador ◽  
Ecological Selection

AbstractEcological speciation occurs when reproductive isolation evolves as a byproduct of adaptive divergence between populations. However, it is unknown whether divergent ecological selection on gene regulation can directly cause reproductive isolation. Selection favoring regulatory divergence between species could result in gene misregulation in F1 hybrids and ultimately lower hybrid fitness. We combined 58 resequenced genomes with 124 transcriptomes to test this hypothesis in a young, sympatric radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas, which consists of a dietary generalist and two novel trophic specialists – a molluscivore and a scale-eater. We found more differential gene expression between closely related sympatric specialists than between allopatric generalist populations separated by 1000 km. Intriguingly, 9.6% of genes that were differentially expressed between sympatric species were also misregulated in their F1 hybrids. Consistent with divergent ecological selection causing misregulation, a subset of these genes were in highly differentiated genomic regions and enriched for functions important for trophic specialization, including head, muscle, and brain development. These regions also included genes that showed evidence of hard selective sweeps and were significantly associated with oral jaw length – the most rapidly diversifying skeletal trait in this radiation. Our results indicate that divergent ecological selection in sympatry can cause hybrid gene misregulation which may act as a primary reproductive barrier between nascent species.SignificanceIt is unknown whether the same genes that regulate ecological traits can simultaneously contribute to reproductive barriers between species. We measured gene expression in two trophic specialist species of Cyprinodon pupfishes that rapidly diverged from a generalist ancestor. We found genes differentially expressed between species that also showed extreme expression levels in their hybrid offspring. Many of these genes showed signs of selection and have putative effects on the development of traits that are important for ecological specialization. This suggests that genetic variants contributing to adaptive trait divergence between parental species negatively interact to cause hybrid gene misregulation, potentially producing unfit hybrids. Such loci may be important barriers to gene flow during the early stages of speciation, even in sympatry.

Ecological speciation! Or the lack thereof?This Perspective is based on the author’s J.C. Stevenson Memorial Lecture delivered at the Canadian Conference for Fisheries Research in Halifax, Nova Scotia, January 2008.

2009 ◽  
Vol 66 (8) ◽  
pp. 1383-1398 ◽  
Author(s):  
Andrew P. Hendry
Keyword(s):  
Nova Scotia ◽  
Reproductive Isolation ◽  
Biological Diversity ◽  
Ecological Speciation ◽  
Divergent Selection ◽  
Adaptive Divergence ◽  
Memorial Lecture ◽  
Darwin’S Finches ◽  
Apparent Deviation ◽  
Different Populations

Ecological speciation occurs when adaptation to different environments or resources causes the evolution of reproductive isolation. This process is now thought to be very important in the evolution of biological diversity. Indeed, support for ecological speciation is so often asserted in the literature that one can get the impression of ubiquity. Eager to ride on the coattails of this exciting work, my own research has investigated ecological speciation in guppies, sticklebacks, and Darwin’s finches. Much to my initial dismay, I failed to find simple and strong signatures of ecological speciation in the first two of these systems. Setting aside the possibility of personal incompetence, my apparent deviation from ubiquity might simply reflect an existing literature bias. This bias seems obvious in retrospect given that essentially all published studies of ecological speciation purport to be confirmatory, whereas many cases of divergent selection and adaptive divergence are associated with only weak to modest levels of reproductive isolation. In short, different populations can be arrayed along a continuum from panmixia to complete reproductive isolation. Variation along this continuum might profitably be used for studying factors, outlined herein, that can promote or constrain “progress” toward ecological speciation.

scholarly journals Phenotypic Dimensions of Reproductive Isolation Between Northern and Melissa Blue Butterflies in the Rocky Mountains

2011 ◽  
Vol 33 ◽  
pp. 101-105
Author(s):  
Zachariah Gompert
Keyword(s):  
Reproductive Isolation ◽  
Biological Diversity ◽  
Butterfly Species ◽  
General Importance ◽  
Greater Yellowstone Area ◽  
Single Character ◽  
Character Variation ◽  
Greater Yellowstone ◽  
Species Speciation

Biological diversity results from speciation, which generally involves the splitting of an ancestral species into descendant species due to adaptation to different niches or the evolution of reproductive incompatibilities (Coyne and Orr 2004). The diverse flora and fauna of the world, including the native inhabitants of the Greater Yellowstone Area (GYA), exist as a result of the speciation process. The central role speciation plays in generating biological diversity imbues importance to our understanding of this process. The general importance of a thorough understanding of speciation is amplified because of the current high rates of extinction on the planet. This is because a long term solution to the present extinction crisis will require maintaining the processes that create species (speciation) not simply preventing extinction. However, many central questions regarding speciation remain to be answered. One fundamental question in speciation research is whether diverging species are isolated (i.e., prevented from interbreeding) due to differences in one, a few, or many characters and whether each of these character differences results from different alleles at a few or many genes. For example, speciation and reproductive isolation might involve divergence along multiple phenotypic axes, such as mate preference, habitat use or preference, and phenology (the timing of life-cycle events). Alternatively, isolation could result from differentiation of a single character. I propose to address this question by assessing patterns of variation for a suite of characters across a hybrid zone between two butterfly species. This is possible because patterns of character variation across hybrids zones allow for inferences about reproductive isolation (Barton and Hewitt 1985).

scholarly journals Phenotypic Dimensions of Reproductive Isolation Between Northern and Melissa Blue Butterflies in the Rocky Mountains

2009 ◽  
Vol 32 ◽  
pp. 97-100
Author(s):  
Zachariah Gompert
Keyword(s):  
Reproductive Isolation ◽  
Biological Diversity ◽  
Butterfly Species ◽  
General Importance ◽  
Greater Yellowstone Area ◽  
Single Character ◽  
Character Variation ◽  
Greater Yellowstone ◽  
Species Speciation

Biological diversity results from speciation, which generally involves the splitting of an ancestral species into descendant species due to adaptation to different niches or the evolution of reproductive incompatibilities (Coyne and Orr 2004). The diverse flora and fauna of the world, including the native inhabitants of the Greater Yellowstone Area (GYA), exist as a result of the speciation process. The central role speciation plays in generating biological diversity imbues importance to our understanding of this process. The general importance of a thorough understanding of speciation is amplified because of the current high rates of extinction on the planet. This is because a long term solution to the present extinction crisis will require maintaining the processes that create species (speciation) not simply preventing extinction. However, many central questions regarding speciation remain to be answered. One fundamental question in speciation research is whether diverging species are isolated (i.e., prevented from interbreeding) due to differences in one, a few, or many characters and whether each of these character differences results from different alleles at a few or many genes. For example, speciation and reproductive isolation might involve divergence along multiple phenotypic axes, such as mate preference, habitat use or preference, and phenology (the timing of life-cycle events). Alternatively, isolation could result from differentiation of a single character. I propose to address this question by assessing patterns of variation for a suite of characters across a hybrid zone between two butterfly species. This is possible because patterns of character variation across hybrids zones allow for inferences about reproductive isolation (Barton and Hewitt 1985).

scholarly journals Multi-locus interactions and the build-up of reproductive isolation

2020 ◽  
Vol 375 (1806) ◽  
pp. 20190543 ◽  
Author(s):  
I. Satokangas ◽  
S. H. Martin ◽  
H. Helanterä ◽  
J. Saramäki ◽  
J. Kulmuni
Keyword(s):  
Reproductive Isolation ◽  
Empirical Work ◽  
Hybrid Fitness ◽  
Epistatic Interactions ◽  
Genome Scans ◽  
Theoretical Approaches ◽  
Genome Wide ◽  
Experimental Approaches ◽  
Polymorphism Data

All genes interact with other genes, and their additive effects and epistatic interactions affect an organism's phenotype and fitness. Recent theoretical and empirical work has advanced our understanding of the role of multi-locus interactions in speciation. However, relating different models to one another and to empirical observations is challenging. This review focuses on multi-locus interactions that lead to reproductive isolation (RI) through reduced hybrid fitness. We first review theoretical approaches and show how recent work incorporating a mechanistic understanding of multi-locus interactions recapitulates earlier models, but also makes novel predictions concerning the build-up of RI. These include high variance in the build-up rate of RI among taxa, the emergence of strong incompatibilities producing localized barriers to introgression, and an effect of population size on the build-up of RI. We then review recent experimental approaches to detect multi-locus interactions underlying RI using genomic data. We argue that future studies would benefit from overlapping methods like ancestry disequilibrium scans, genome scans of differentiation and analyses of hybrid gene expression. Finally, we highlight a need for further overlap between theoretical and empirical work, and approaches that predict what kind of patterns multi-locus interactions resulting in incompatibilities will leave in genome-wide polymorphism data. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

scholarly journals Cytonuclear Genetic Incompatibilities in Plant Speciation

Plants ◽  
2020 ◽  
Vol 9 (4) ◽  
pp. 487 ◽  
Author(s):  
Zoé Postel ◽  
Pascal Touzet
Keyword(s):  
Reproductive Isolation ◽  
Plant Species ◽  
Mating Systems ◽  
Cell Function ◽  
Evolutionary Processes ◽  
Hybrid Fitness ◽  
Plant Mating Systems ◽  
The Impact ◽  
Cytonuclear Interaction ◽  
Endosymbiotic Origin

Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation.

scholarly journals Limited intrinsic postzygotic reproductive isolation despite chromosomal rearrangements between closely related sympatric species of small ermine moths (Lepidoptera: Yponomeutidae)

2019 ◽  
Vol 128 (1) ◽  
pp. 44-58 ◽  
Author(s):  
Katerina H Hora ◽  
František Marec ◽  
Peter Roessingh ◽  
Steph B J Menken
Keyword(s):  
Reproductive Isolation ◽  
Parental Species ◽  
Meiotic Chromosome ◽  
Chromosomal Rearrangements ◽  
Sympatric Species ◽  
Hybrid Fitness ◽  
New Host ◽  
Closely Related Species ◽  
Postzygotic Reproductive Isolation

Abstract In evolutionarily young species and sympatric host races of phytophagous insects, postzygotic incompatibility is often not yet fully developed, but reduced fitness of hybrids is thought to facilitate further divergence. However, empirical evidence supporting this hypothesis is limited. To assess the role of reduced hybrid fitness, we studied meiosis and fertility in hybrids of two closely related small ermine moths, Yponomeuta padella and Yponomeuta cagnagella, and determined the extent of intrinsic postzygotic reproductive isolation. We found extensive rearrangements between the karyotypes of the two species and irregularities in meiotic chromosome pairing in their hybrids. The fertility of reciprocal F1 and, surprisingly, also of backcrosses with both parental species was not significantly decreased compared with intraspecific offspring. The results indicate that intrinsic postzygotic reproductive isolation between these closely related species is limited. We conclude that the observed chromosomal rearrangements are probably not the result of an accumulation of postzygotic incompatibilities preventing hybridization. Alternative explanations, such as adaptation to new host plants, are discussed.

scholarly journals Male-Female Interactions and the Evolution of Postmating Prezygotic Reproductive Isolation among Species of the Virilis Subgroup

2011 ◽  
Vol 2011 ◽  
pp. 1-11 ◽  
Author(s):  
Nada Sagga ◽  
Alberto Civetta
Keyword(s):  
Reproductive Isolation ◽  
Egg Laying ◽  
Sperm Transfer ◽  
Geographic Locations ◽  
Future Studies ◽  
Egg Hatchability ◽  
Fertilization Rates ◽  
Postzygotic Barriers ◽  
Storage Organs

Reproductive isolation reduces breeding between species. Traditionally, prezygotic and postzygotic barriers to reproduction have been broadly studied, but in recent years, attention has been brought to the existence of barriers that act after copulation but before fertilization. Here, we show that when D. virilis females from different geographic locations mate with D. novamexicana males, egg laying is normal, but fertilization rates are severely reduced, despite normal rates of sperm transfer. This reduction in fertilization is probably due to lower retention of heterospecific sperm in female storage organs one-to-two days after copulation. An inspection of egg hatchability in crosses between females and males from other virilis subgroup species reveals that isolation due to poor egg hatchability likely evolved during the diversification of D. virilis/D. lummei from species of the novamexicana-americana clade. Interestingly, the number of eggs laid by D. virilis females in heterospecific crosses was not different from the numbers of eggs laid in conspecific crosses, suggesting that females exert some form of cryptic control over the heterospecific ejaculate and that future studies should focus on how female and female-sperm interactions contribute to the loss or active exclusion of heterospecific sperm from storage.

THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION IN LOUISIANA IRISES: HYBRID FITNESS IN NATURE

Evolution ◽  
2009 ◽  
Vol 63 (10) ◽  
pp. 2581-2594 ◽  
Author(s):  
Sunni J. Taylor ◽  
Michael Arnold ◽  
Noland H. Martin
Keyword(s):  
Reproductive Isolation ◽  
Genetic Architecture ◽  
Hybrid Fitness
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