Facultative pupal mating in <i>Heliconius erato</i>: Implications for mate choice, female preference, and speciation

Thurman, Timothy J.; Brodie, Emily G.; Evans, Elizabeth; McMillan, W. Owen

doi:10.1002/ece3.3624

Cited by 18 publications

(16 citation statements)

References 47 publications

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“…higher than in monandrous species and adult mating is likely still prevalent in presumed pupal-mating species (Thurman, Brodie, Evans, & McMillan, 2018). Correspondingly, we did not find any clear difference in Z/A diversity ratios between the pupal-mating H. erato and adult-mating H. melpomene clade populations (Figure 7).…”

Section: Alternative Factors Affecting Z/a Diversity Ratios In Helimentioning

confidence: 47%

“…Such differences in mating system could potentially result in increased variance of male reproductive success and decreased Z/A diversity ratios for monandrous mating systems (Charlesworth, ). However, the frequency of remating in polyandrous Heliconius species is estimated to be only 25–30% higher than in monandrous species (Walters et al., ) and adult mating is likely still prevalent in presumed pupal‐mating species (Thurman, Brodie, Evans, & McMillan, ). Correspondingly, we did not find any clear difference in Z/A diversity ratios between the pupal‐mating H. erato and adult‐mating H. melpomene clade populations (Figure ).…”

Section: Resultsmentioning

confidence: 99%

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Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

et al. 2018

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Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a ‘large-X’ effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. ‘faster-X’, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of incompatibilities. Our work demonstrates the importance of taking demography into account in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

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Section: Alternative Factors Affecting Z/a Diversity Ratios In Helimentioning

confidence: 47%

Section: Resultsmentioning

confidence: 99%

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

et al. 2018

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“…Indirect evidence of mating cost related to female immobility is provided in Heliconius species with facultative pupal–adult mating; pupal–adult mating is characterized by males being attracted to the scent of female pupae shortly before emergence, such that males copulate when females are still partly enclosed in their pupal case. Sentinel individuals released as larva and allowed to mate as pupa largely failed to do so (two of 11 mated females, or 18.2%); in contrast, all females released as mobile adults mated at least once (Thurman et al., ). Low mating success of tethered females relative to feral females in field experiments is also consistent with a mating cost associated with restricted mobility (Rhainds, ).…”

Section: The Role Of Immobility In Fmfmentioning

confidence: 99%

Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids

Rhainds

2019

Entomologia Exp Applicata

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Sexual reproduction implies binary outcomes of competitive interactions for access to male gametes: lifelong virgin females with null fitness vs. mated females with variable (generally nonzero) fitness. Female mating failure has long remained a dormant concept in sexual selection theory in part because it is acutely maladaptive (lifelong virgins that do not reproduce are strongly selected against) and also due to widespread acceptance of the Bateman–Trivers paradigm (anisogamy and correlated sex roles). Based on recent scientific output on lifelong virginity across multiple taxonomic groups in insects (Coleoptera, Diptera, Hemiptera, Lepidoptera, Odonata, Orthoptera, Strepsiptera), female mating failure has become a mainstay of sexual selection over the last decade. Lifelong virginity and senescence (death) are intertwined processes; old virgin females compensate for increased risk of lifelong virginity by becoming less choosy and increasing investment in mating‐related activities. Low rates of female lifelong virginity (<5%) in most natural populations of insects indicate that sex generally ‘works’ due to selective pressures acting on both males and females to enhance lifetime fitness. Mating failures are most common in insects with female flightlessness; these pressures may lead in evolutionary time to transitionary pathways from sexual reproduction to parthenogenesis. Female mating probability is affected by nonlinear density‐dependent processes dependent upon the scale of observation (mate‐encounter Allee effect at large spatial scales, mating interferences between females at small scales). Mate choice and sex role reversal (females being the active sexual partner) are ubiquitous in insects and arachnids with significant paternal investment, but consequences in terms of female lifelong virginity remain unknown. Logistically, conceptual development of female mating failure in insects is most limited by the lack of broadly applicable methods to assess rates of lifetime virginity among flighted females.

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“…Butterflies have served as a historically significant model of insect diversity because of the group's extreme species diversity, containing an estimated 18,000 species, and the even more striking color pattern diversity that defines the subspecies, races, forms, and morphs of many butterfly species. Among butterflies, the Neotropical genus Heliconius has attracted attention for centuries because of their bold and highly variable wing color patterns [1][2][3][4], as well as their fascinating behavior and natural history, which includes co-evolved relationships with larval host plants, widespread Müllerian mimicry, adult pollen feeding, and pupal-mating behavior [2,[4][5][6]. Today, researchers are leveraging the natural diversity of Heliconius butterflies and genomic tools to characterize the molecular genetic basis of mimicry [7][8][9][10][11][12][13] and track genome-wide patterns of differentiation and introgression associated with speciation [14][15][16][17][18][19][20].…”

Section: Introductionmentioning

confidence: 99%

The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

et al. 2020

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Background: Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri. Results: We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato, of a small genomic region upstream of the color patterning gene cortex. Conclusions: Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.

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Facultative pupal mating in Heliconius erato: Implications for mate choice, female preference, and speciation

Cited by 18 publications

References 47 publications

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids

The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

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