scholarly journals Patterns of hybrid seed inviability in perennials of the Mimulus guttatus sp. complex reveal a potential role of parental conflict in reproductive isolation

2018 ◽  
Author(s):  
Jenn M. Coughlan ◽  
Maya Wilson Brown ◽  
John H. Willis

SummaryGenomic conflicts may play a central role in the evolution of reproductive barriers. Theory predicts that early-onset hybrid inviability may stem from conflict between parents for resource allocation to offspring. Here we describe M. decorus; a group of cryptic species within the M. guttatus species complex that are largely reproductively isolated by hybrid seed inviability (HSI). HSI between M. guttatus and M. decorus is common and strong, but populations of M. decorus vary in the magnitude and directionality of HSI with M. guttatus. Patterns of HSI between M. guttatus and M. decorus, as well as within M. decorus conform to the predictions of parental conflict: (1) reciprocal F1s exhibit size differences and parent-of-origin specific endosperm defects, (2) the extent of asymmetry between reciprocal F1 seed size is correlated with asymmetry in HSI, and (3) inferred differences in the extent of conflict predict the extent of HSI between populations. We also find that HSI is rapidly evolving, as populations that exhibit the most HSI are each others’ closest relative. Lastly, while all populations are largely outcrossing, we find that the differences in the inferred strength of conflict scale positively with π, suggesting that demographic or life history factors other than mating system may also influence the rate of parental conflict driven evolution. Overall, these patterns suggest the rapid evolution of parent-of-origin specific resource allocation alleles coincident with HSI within and between M. guttatus and M. decorus. Parental conflict may therefore be an important evolutionary driver of reproductive isolation.

2018 ◽  
Author(s):  
Jenn M. Coughlan ◽  
John H. Willis

SummaryRationaleHybrid seed inviability (HSI) is a common reproductive barrier in angiosperms, yet the evolutionary and developmental drivers of HSI remain largely unknown. We test whether conflict between maternal and paternal interests in resource allocation to developing offspring (i.e. parental conflict) are associated with HSI and determine the degree of developmental parallelism between independent incidences of HSI in Mimulus.MethodsWe quantified HSI between M. guttatus and two clades of M. decorus with oppositely asymmetric incompatibilities and surveyed development of hybrid and parental seeds.Key ResultsCrosses between M. guttatus and both clades of M. decorus show parent-of-origin effects on reciprocal F1 seed development, but in opposing directions. Inviable hybrid seeds exhibit paternal excess phenotypes, wherein endosperm is large and chaotic while viable hybrid seeds produce endosperm cells that are smaller and less prolific (i.e. maternal-excess phenotypes).Main ConclusionsWe find strong parent-of-origin effects on development in reciprocal F1s in multiple incidences of HSI in Mimulus. These patterns suggest that parental conflict may be an important force generating HSI in this group, and mismatches between maternal and paternal contributions to developing seeds result in repeatable developmental defects in hybrids.


Genome ◽  
2020 ◽  
pp. 1-11
Author(s):  
Bahar Patlar ◽  
Alberto Civetta

It has long been acknowledged that changes in the regulation of gene expression may account for major organismal differences. However, we still do not fully understand how changes in gene expression evolve and how do such changes influence organisms’ differences. We are even less aware of the impact such changes might have in restricting gene flow between species. Here, we focus on studies of gene expression and speciation in the Drosophila model. We review studies that have identified gene interactions in post-mating reproductive isolation and speciation, particularly those that modulate male gene expression. We also address studies that have experimentally manipulated changes in gene expression to test their effect in post-mating reproductive isolation. We highlight the need for a more in-depth analysis of the role of selection causing disrupted gene expression of such candidate genes in sterile/inviable hybrids. Moreover, we discuss the relevance to incorporate more routinely assays that simultaneously evaluate the potential effects of environmental factors and genetic background in modulating plastic responses in male genes and their potential role in speciation.


Zootaxa ◽  
2021 ◽  
Vol 5061 (3) ◽  
pp. 523-544
Author(s):  
BRUNA EMILIA ROMAN ◽  
LILIAN MADI-RAVAZZI

Male terminalia in insects with internal fertilization evolve more rapidly than other structures. The aedeagus is the most variable structure, making it a valuable diagnostic feature to distinguish species. The saltans group Sturtevant of Drosophila Fallén contains sibling species, that can be distinguished by their aedeagi. Here, we revised and illustrated the morphology of the male terminalia of the following species: Drosophila prosaltans Duda, 1927; D. saltans Sturtevant, 1916; D. lusaltans Magalhães, 1962; D. austrosaltans Spassky, 1957; D. septentriosaltans Magalhães, 1962; D. nigrosaltans Magalhães, 1962; D. pseudosaltans Magalhães, 1956; D. sturtevanti Duda, 1927; D. lehrmanae Madi-Ravazzi et al., 2021; D. dacunhai Mourão & Bicudo, 1967; D. milleri Magalhães, 1962; D. parasaltans Magalhães, 1956; D. emarginata Sturtevant, 1942; D. neoelliptica Pavan & Magalhães in Pavan, 1950; D. neosaltans Pavan & Magalhães in Pavan, 1950 and D. neocordata Magalhães, 1956. We found that phallic structures (e.g., the aedeagus) evolve more rapidly than periphallic structures (e.g., epandrium), being completely different among the subgroups and within them. This rapid evolution may be due to the action of sexual selection or to the potential role of those structures in speciation.  


2019 ◽  
Author(s):  
P. Brand ◽  
I. A. Hinojosa-Díaz ◽  
R. Ayala ◽  
M. Daigle ◽  
C. L. Yurrita Obiols ◽  
...  

Speciation is facilitated by the evolution of reproductive barriers that prevent or reduce hybridization among diverging lineages. However, the genetic mechanisms that control the evolution of reproductive barriers remain elusive, particularly in natural populations. We identify a gene associated with divergence in chemical courtship signaling in a pair of nascent orchid bee lineages. Male orchid bees collect perfume compounds from flowers and other sources to subsequently expose during courtship display, thereby conveying information on species identity. We show that these two lineages exhibit differentiated perfume blends and that this change is associated with the rapid evolution of a single odorant receptor gene. Our study suggests that reproductive isolation evolved through divergence of a major barrier gene involved in chemically mediated pre-mating isolation via genetic coupling.


2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Yukie Sato ◽  
Satoshi Fujiwara ◽  
Martijn Egas ◽  
Tomoko Matsuda ◽  
Tetsuo Gotoh

Abstract Background Evolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher). Results We sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0–99.9% barrier) at genetic distances of 0.475–0.657, 0.150–0.209 and 0.145–0.210, respectively. Besides, we found asymmetries in reproductive isolation. Conclusions The prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this study and previous work, a genetic distance of 0.15–0.21 in mtDNA (COI) appears required for speciation in spider mites. Variations and asymmetries in the degree of reproductive isolation highlight the importance of reinforcement of prezygotic reproductive isolation through incompatibility and the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.


2019 ◽  
Vol 128 (4) ◽  
pp. 779-788 ◽  
Author(s):  
Donald R Forsdyke

Abstract Animal gametes unite to form a zygote that develops into an adult with gonads that, in turn, produce gametes. Interruption of this germinal cycle by prezygotic or postzygotic reproductive barriers can result in two cycles, each with the potential to evolve into a new species. When the speciation process is complete, members of each species are fully reproductively isolated from those of the other. During speciation a primary barrier may be supported and eventually superceded by a later-appearing secondary barrier. For those holding certain cases of prezygotic isolation to be primary (e.g. elephant cannot copulate with mouse), the onus is to show that they had not been preceded over evolutionary time by periods of postzygotic hybrid inviability (genically determined) or sterility (genically or chromosomally determined). Likewise, the onus is upon those holding cases of hybrid inviability to be primary (e.g. Dobzhansky–Muller epistatic incompatibilities) to show that they had not been preceded by periods, however brief, of hybrid sterility. The latter, when acting as a sympatric barrier causing reproductive isolation, can only be primary. In many cases, hybrid sterility may result from incompatibilities between parental chromosomes that attempt to pair during meiosis in the gonad of their offspring (Winge-Crowther-Bateson incompatibilities). While such incompatibilities have long been observed on a microscopic scale, there is growing evidence for a role of dispersed finer DNA sequence differences (i.e. in base k-mers).


2020 ◽  
Vol 126 (6) ◽  
pp. 991-1003 ◽  
Author(s):  
Mariana Castro ◽  
João Loureiro ◽  
Brian C Husband ◽  
Sílvia Castro

Abstract Background and Aims Polyploidy is an important contributor to sympatric speciation and assortative mating is a key mechanism driving cytotype interactions in contact zones. While strong reproductive barriers can mediate the coexistence of different cytotypes in sympatry, positive frequency-dependent mating disadvantage ultimately drives the transition to single-ploidy populations. However, comprehensive estimates of reproductive isolation among cytotypes and across multiple barriers are rare. We quantify the strength of isolation across multiple reproductive stages in a tetraploid–octoploid contact zone to understand the potential for coexistence. Methods Assortative mating due to flowering asynchrony, pollinator behaviour, morphological overlap, self-fertilization and gametic competition between tetraploid and octoploid Gladiolus communis in a contact zone in the Western Iberian Peninsula were assessed in natural and experimental populations to quantify reproductive isolation (RI) between cytotypes. Key Results Tetraploids and octoploids have a high degree of overlap in flowering time and similar floral morphology, and are visited by generalist insects without cytotype foraging preferences, resulting in weak pre-pollination RI (from 0.00 to 0.21). In contrast, post-pollination isolation resulting from gametic selection was a strong barrier to inter-cytotype mating, with ploidy composition in stigmatic pollen loads determining the levels of RI (from 0.54 to 1.00). Between-cytotype cross-incompatibility was relatively high (RI from 0.54 to 0.63) as was isolation acquired through self-pollination (RI of 0.59 in tetraploids and 0.39 in octoploids). Conclusions Total RI was high for both tetraploids (from 0.90 to 1.00) and octoploids (from 0.78 to 0.98). Such high rates of assortative mating will enable cytotype coexistence in mixed-ploidy populations by weakening the impacts of minority cytotype exclusion. This study reveals the key role of gametic selection in cytotype siring success and highlights the importance of comprehensive estimates across multiple reproductive barriers to understand cytotype interactions at contact zones.


2013 ◽  
Vol 59 (5) ◽  
pp. 591-603 ◽  
Author(s):  
Alycia C. R. Lackey ◽  
Janette Wenrick Boughman

Abstract One approach to understand the importance of reproductive barriers to the speciation process is to study the breakdown of barriers between formerly distinct species. One reproductive barrier, sexual isolation, reduces gene flow between species through differences in mate preferences and mating signals and is likely important for species formation and maintenance. We measure sexual isolation in two limnetic-benthic threespine stickleback species pairs (Gasterosteus spp.). One species pair maintains strong reproductive isolation while the other species pair has recently collapsed into a hybrid swarm. We compare the strength of sexual isolation in the hybridizing pair to the currently isolated pair. We provide the first evidence that sexual isolation has been lost in the hybridizing pair and show furthermore that preferences females have for conspecific mates and the traits they use to distinguish conspecific and heterospecific males contribute to this loss. This work highlights the fragility of reproductive isolation between young species pairs and considers the role of sexual isolation in speciation.


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