Figure 3 - uploaded by Bengt Karlsson
Content may be subject to copyright.
Number of eggs laid by female Pieris napi in relation to the amount of nutrients (DPM, disintegrations per minute) received from males (r = 0.73, p = 0.0001, n = 22).
Source publication
Female reproductive effort can be influenced by the quality of her mate. In some species, females increase their reproductive effort by differentially allocating resources after mating with high-quality males. Examination of female reproductive effort in relation to male quality has implications for estimating the evolvability of traits and for sex...
Context in source publication
Context 1
... increased investment by Pieris napi females after receiving larger donations from the male is expressed by the production of more eggs ( figure 3). However, Pieris napi females do not appear to increase their investment in each individual egg in relation to the amount of resources provided by the male. ...
Citations
... One could predict that a male or a female modulates its investment in reproduction based on the MHC quality of its mate (Sheldon, 2000;Wedell & Karlsson, 2003;Zelano & Edwards, 2002). To the best of our knowledge, the only study that explores this question was conducted on blue peafowl, Pavo cristatus (Hale et al., 2009). ...
The selective pressure from pathogens on individuals can have direct consequences on reproduction. Genes from the major histocompatibility complex (MHC) are central to the vertebrate adaptive immune system and pathogen resistance. In species with biparental care, each sex has distinct reproductive roles and levels of investment, and due to a trade‐off with immunity, one can expect different selective regimes acting upon the MHC of each parent. Here, we addressed whether couples combine each other's variation at MHC loci to increase their breeding success. Specifically, we used a 23‐year dataset from a barn owl population ( Tyto alba ) to understand how MHC class Iα and IIβ functional divergence and supertypes of each parent were associated with clutch size and fledging success. We did not detect associations between MHC diversity and supertypes with the clutch size or with the fledging success. In addition, to understand the relative contribution from the MHC of the genetic parents and the social parents, we analyzed the fledging success using only a cross‐fostered dataset. We found several associations of weak‐to‐moderate effect sizes between the father's MHC and fledging success: (i) lower MHC‐Iα divergence in the genetic father increases fledging success, which might improve paternal care during incubation, and (ii) one and two MHC‐IIβ DAB2 supertypes in the social father decrease and increase, respectively, fledging success, which may affect the paternal care after hatching. Furthermore, fledging success increased when both parents did not carry MHC‐IIβ DAB1 supertype 2, which could suggest conditional effects of this supertype. Although our study relied on a substantial dataset, we showed that the associations between MHC diversity and reproductive success remain scarce and of complex interpretation in the barn owl. Moreover, our results highlighted the need to incorporate more than one proxy of reproductive success and several MHC classes to capture more complex associations.
... Organisms constantly face trade-offs in resource allocation toward various traits to survive and reproduce successfully (Contreras-Garduño et al., 2006;Lin et al., 2016;Loiseau et al., 2008;Mangel & Heimpel, 1998;Peck et al., 2016;Verhulst et al., 2005;Wedell & Karlsson, 2003). Individuals maximize fitness by allocating optimal amounts of reserves toward various life-history activities and states. ...
Sexes of a species may show different characteristics beyond the differences in their sexual organs and such sexual dimorphism often occurs in the level of immune response when exposed to pathogens (immunocompetence). In general, females have increased longevity relative to males, which is associated with higher immunocompetence. However, males have higher immunocompetence in some species, such as pipefishes and seahorses. Experimental evidence suggests that this could be because males, rather than females, carry fertilized eggs to birth in these species. This observation suggests that an increase in immunocompetence may be related to the level of parental investment and not to a particular sex. We use state‐dependent life‐history theory to study optimal investment in offspring production relative to parent immunocompetence, varying the relative time that a parent spends in brooding or pregnancy within a breeding cycle. When offspring is dependent on a parent's survival for a large part of the breeding cycle, we predict higher investments in immunity and longer life expectancies.
... In response, females might evolve organs that efficiently digest each nuptial gift to allow for multiple mating and the avoidance of the fertilization of all the eggs by a unique genitor (Lewis et al., 2020). Additionally, as the nutrients received from the males can be upcycled towards the production of eggs, or of better-quality eggs (Wedell & Karlsson, 2003), females might engage in female-female conflicts, and evolve organs that also optimise the intake from the nuptial gift (Meslin et al., 2017), especially in population where males transfer small spermatophores. ...
Background
Sexual selection and conflicts within and between sexes promote morphological diversity of reproductive traits within species. Variation in the morphology of diagnostic reproductive characters within species offer an excellent opportunity to study these evolutionary processes as drivers of species diversification. The African monarch, Danaus chrysippus (Linnaeus, 1758), is widespread across Africa. The species is polytypic, with the respective geographical ranges of the four colour morphs only overlapping in East Africa. Furthermore, some of the populations host an endosymbiotic bacterium, Spiroplasma , which induces son-killing and distorts the local host population sex-ratio, creating sexual conflicts between the females seeking to optimize their fecundity and the limited mating capacity of the rare males.
Methods
We dissected females from Kenya, Rwanda and South Africa, where Spiroplasma vary in presence and prevalence (high, variable and absent, respectively), and conducted microscopy imaging of their reproductive organs. We then characterized the effect of population, female body size, and female mating status, on the size and shape of different genitalia characters of the D. chrysippus female butterflies.
Results
We showed that although the general morphology of the organs is conserved in D. chrysippus , female genitalia vary in size and shape between and within populations. The virgin females have smaller organs, while the same organs were expanded in mated females. Females from highly female-biased populations, where the male-killing Spiroplasma is prevalent, also have a larger area of their corpus bursae covered with signa structures. However, this pattern occurs because a larger proportion of the females remains virgin in the female-biased populations rather than because of male depletion due to the symbiont, as males from sex-ratio distorted populations did not produce significantly smaller nutritious spermatophores.
... In scenario (II), females receive small or few spermatophores in their lifetime. As the nutrients received from the males can be upcycled towards the production of eggs, or of better-quality eggs 41 , females would evolve organs to optimise the intake from the small nuptial gift 42 . ...
Sexual selection, and conflicts between sex or within sex, can induce morphological variations within species. This may challenge the identification and characterization of diagnostic morphological characters from reproductive organs that are of utmost importance for the morphology-based classification of faunal diversity, particularly on species level. In Lepidoptera, and in some other insects, females have evolved reproductive organs that can accommodate and/or digest nuptial gifts, or so called spermatophores, transferred from the males during copulation. The properties of the spermatophores principally depend on the male’s condition, which is defined by resources acquired and depleted across life stages. In these conditions, the size and/or shape of the female reproductive organs are likely to differ visually between females of different mating status, and with their mates’ condition. The widespread African monarch, Danaus chrysippus , can host an endosymbiotic bacterium, Spiroplasma that induces son-killing in this species. When prevalent, such symbionts distort their host population sex-ratio, which can increase the reproduction load on the few uninfected males, lead to a local excess of unmated females, and resource-depletion in males. Here, we characterized variation in the female genitalia across populations with different levels of Spiroplasma infection. First, virgin females have smaller organs, while mated females show expanded organs; and further, females from highly female-biased and male-killing Spiroplasma infected populations have a larger area of their corpus bursae covered with signa structures. These observations potentially suggest that females from populations that are male depleted may have evolved an efficient mechanical way to optimize the digestion of small nutritious spermatophores.
... While providing an additional source of macronutrients for adult females, nuptial gifts have the potential to both ameliorate and magnify flight-fecundity trade-offs. In Pierids, a single nuptial gift can provide the necessary nutrients to produce 50-80 eggs, a substantial contribution to female fecundity (Karlsson, 1998;Wiklund et al., 1998;Wedell and Karlsson, 2003). Amino acids supplied through nuptial gifts can change female reliance on amino acid-rich nectar preference (Mevi-Schütz and Erhardt, 2003), which may affect the pollination efficiency of the female. ...
Plant–herbivore and plant–pollinator interactions are both well-studied, but largely independent of each other. It has become increasingly recognized, however, that pollination and herbivory interact extensively in nature, with consequences for plant fitness. Here, we explore the idea that trade-offs in investment in insect flight and reproduction may be a mechanistic link between pollination and herbivory. We first provide a general background on trade-offs between flight and fecundity in insects. We then focus on Lepidoptera; larvae are generally herbivores while most adults are pollinators, making them ideal to study these links. Increased allocation of resources to flight, we argue, potentially increases a Lepidopteran insect pollinator’s efficiency, resulting in higher plant fitness. In contrast, allocation of resources to reproduction in the same insect species reduces plant fitness, because it leads to an increase in herbivore population size. We examine the sequence of resource pools available to herbivorous Lepidopteran larvae (maternally provided nutrients to the eggs, as well as leaf tissue), and to adults (nectar and nuptial gifts provided by the males to the females), which potentially are pollinators. Last, we discuss how subsequent acquisition and allocation of resources from these pools may alter flight–fecundity trade-offs, with concomitant effects both on pollinator performance and the performance of larval herbivores in the next generation. Allocation decisions at different times during ontogeny translate into costs of herbivory and/or benefits of pollination for plants, mechanistically linking herbivory and pollination.
... During mating, male Lepidoptera transfer a spermatophore, which may vary in size and content due to several non-exclusive factors that include the mass of the male, age, past mating history, and the duration of mating [21,[24][25][26]. In turn, the size of the spermatophore may influence female reproductive success, as larger ones generally contain more sperm and nutrients than smaller ones [27,28], resulting in females producing more eggs [29] with a higher incidence of hatching [30]. ...
... The reduction in spermatophore size did not result in a decrease in the total number of eggs laid by RR females (Figure 4) but there was a significant reduction in the proportion of hatching ( Figure 5). Additional research will be required to determine to what extent this is due to the number and/or quality of sperm and male accessory gland secretions produced, as all of these parameters have been shown to affect fertility in other species [22,26,27,29,40]. However, one cannot eliminate possible female effects relating to the transfer of sperm from the bursa copulatrix to the spermatheca [41][42][43] or the fertilization of eggs during oviposition [23]. ...
The fall armyworm (FAW) Spodoptera frugiperda is the most significant lepidopteran corn pest in South American countries. Transgenic Bt corn, producing the Cry1Fa toxins, has been used to control this pest, but there is clear evidence that some FAW populations have developed resistance. To determine if there are costs associated with resistance, we compared the mass of adults, the duration of mating, and the mass of the first spermatophore produced, as well as the lifetime fecundity and fertility of once-mated susceptible (SS) and resistant (RR) females. Adult mass was affected by both sex and strain, with SS females being significantly larger than RR ones, while the inverse was true for males. RR pairs took significantly longer to mate than SS pairs, yet the mass of spermatophores produced by RR males was significantly less than those of SS males. The total number of eggs laid did not differ but the fertility of eggs from once-mated RR pairs was significantly lower than that of SS pairs. Our data provided clear evidence that the development of Bt resistance affected the reproductive capacity of resistant FAW.
... This change in reproductive strategy (i.e., increased investment in current reproduction rather than in future reproduction) by warm-exposed males may be mediated by a higher investment in sperm quality, rather than in nuptial gifts. It is noteworthy, however, that while spermatophore content (Wedell & Karlsson, 2003;Wiklund et al., 1993) and/or the presence of additional male-delivered nutrients are known to increase female fecundity in other Lepidoptera (Boggs & Gilbert, 1979), larger spermatophores in the Glanville fritillary butterfly do not increase paternity chances or male fertilization success (Duplouy et al., 2018). ...
Warming temperatures are greatly impacting wild organisms across the globe. Some of the negative impacts of climate change can be mitigated behaviorally, for example, by changes in habitat and oviposition site choice. Temperatures are reportedly warming faster at night than during the day, yet studies assessing the impacts of increasing night temperature are rare. We used the Finnish Glanville fritillary butterfly (Melitaea cinxia) as study species and exposed adult butterflies of both sexes to warmer night conditions. Under a seminatural outdoor enclosure, we assessed whether females base their oviposition choices primarily on habitat site characteristics (open, suggestive of dry meadows, versus covered by a coarse canopy, suggestive of pastures) or on plant condition (dry vs. lush), and if their choice is altered by the thermal conditions experienced at night. As exposure to warmer environmental conditions is expected to increase resting metabolic rate and potentially reduce life expectancy, we further assessed the fitness implications of warm-night temperatures. We found that females prefer open sites for oviposition and that females do not switch their oviposition strategy based on the thermal conditions they experienced at night prior to the reproductive event. Exposure to warm nights did not influence female lifespan, but the egg hatching success of their offspring was reduced. In addition, we found that males exposed to warm nights sired larger clutches with higher hatching rate. As warm-night exposure reduced male lifespan, this may imply a switch in male resource allocation strategy toward increased offspring quality. The present work adds on to the complex implications of climate warming and highlights the importance of the often-neglected role of males in shaping offspring performance.
... We additionally investigated potential differences in the number of times females mated depending on their larval nutrition treatment, since spermatophore nutrients can supplement adult nutrition Wedell and Karlsson 2003) and energy available for reproduction and flight (Watanabe and Ando 1993;Watanabe 1988, Oberhauser 1989. We followed the same dissection protocol as for egg measurements (detailed above). ...
... Females could also partially compensate for nutritional deficits through spermatophores acquired from males during mating. Nutrients from male spermatophores are known to contribute to egg development and maturation in pierids and other butterflies Gilbert 1979, Wedell andKarlsson 2003), boosting fecundity and egg size (Watanabe 1988, Watanabe and Ando 1993, Oberhauser 1989. Similarly, female butterflies in our study could have partially compensated for poor larval nutrition, or even poor adult nutrition, through nutrients acquired from multiple spermatophores. ...
Despite the benefits of careful decision-making, not all animals are choosy. One explanation is that choosiness can cost time and energy and thus depend on nutrition. However, it is not clear how allocation to choosiness versus other components of life-history shifts in the face of nutritional stress. We tested 2 hypotheses about the effects of nutritional stress on choosiness and other life-history traits: 1) poor nutrition leads to compensatory shifts in life-history strategy towards greater investment per offspring in terms of choosy oviposition behavior and egg resources, and 2) poor nutrition negatively affects a range of life-history traits. Cabbage white butterfly (Pieris rapae) females were reared under low or high nutrition conditions during the larval and adult stage in a fully factorial design. Choosiness was quantified as avoidance of conspecific models during oviposition. Adult life-history traits included egg number, egg size, and thorax protein. Females that experienced nutritional stress as adults were less choosy and less fecund, in support of the second hypothesis. Yet females that were stressed as larvae invested more in thorax muscle, consistent with the first hypothesis. Overall, adult nutritional stress decreased investment in multiple reproductive traits, including a behavioral trait, but larval stress increased investment in flight, potentially to disperse away from nutritionally poor environments.
... Sperm and other ejaculate 48 components contain a variety of nutrients and have a high concentration of protein (Dewsbury 49 1982;Wedell et al. 2002). Moreover, many males provide females with nitrogen-rich nuptial gifts 50 during mating, which may have important nutritional value to survival and growth of developing 51 embryos (Vahed 1998;Wedell and Karlsson 2003;Gwynne 2008). Gifts may contain protein or 52 inorganic nitrogen derived from protein that can be used for protein synthesis by the female 53 (Mullins and Keil 1980;Voigt et al. 2006;Patiño-Navarrete et al. 2014). ...
Protein is an abundant nutrient in sperm, and males therefore expend protein every time they mate. In addition, many males provide the female with a nitrogen-rich nuptial gift during mating, which often increases female fertility by supplementing her pool of limiting nutrients. However, it is unknown whether males compensate for the nitrogen cost of mating by increasing their preference for protein, which would facilitate the production of new sperm and nuptial gift material. Using artificial diets, we investigated whether male German cockroaches (Blattella germanica) would compensate for nitrogen expenses of mating by increasing protein preference when given the opportunity to self-select their diet from complementary foods differing only in protein and carbohydrate content. We distributed adult males across 4 mating regimes differing in the frequency of mating opportunities with receptive females and measured protein and carbohydrate consumption as well as reproductive output over the lifespan of each male. Receptive females were either never available (no mating opportunity), or they were available overnight at a frequency of each 28 days (rare mating opportunities), each 14 days (occasional mating opportunities), or each 7 days (frequent mating opportunities). Males selected highly carbohydrate-biased diets. However, males that mated more frequently had higher consumption and reproduction and self-selected higher lifetime protein to carbohydrate ratios. Our study demonstrates that male German cockroaches actively select a more protein-biased diet that compensates for their nutritional requirements following mating. The study shows that male mating significantly affects foraging decisions for specific nutrients to compensate for the expenses of mating.
... These include: males that contribute little to care have more time to sequester new mating opportunities (Kokko & Jennions, 2008;Fromhage & Jennions, 2016); intense mate-guarding selects for more substantial male care contributions, since mate-guarding restricts the chances of additional mating opportunities (van Rhijn, 1991;Kokko & Jennions, 2008;Fromhage & Jennions, 2016); and if females benefit from mating with high-quality carers, not just due to direct but also indirect benefits (cf . Wedell & Karlsson, 2003;Miller & Moore, 2007), they would be expected to seek fewer extra-pair copulations when mated to such males. ...
Why do some animals mate with one partner rather than many? Here, I investigate factors related to (i) spatial constraints (habitat limitation, mate availability), (ii) time constraints (breeding synchrony, length of breeding season), (iii) need for parental care, and (iv) genetic compatibility, to see what support can be found in different taxa regarding the importance of these factors in explaining the occurrence of monogamy, whether shown by one sex (monogyny or monandry) or by both sexes (mutual monogamy). Focusing on reproductive rather than social monogamy whenever possible, I review the empirical literature for birds, mammals and fishes, with occasional examples from other taxa. Each of these factors can explain mating patterns in some taxa, but not in all. In general, there is mixed support for how well the factors listed above predict monogamy. The factor that shows greatest support across taxa is habitat limitation. By contrast, while a need for parental care might explain monogamy in freshwater fishes and birds, there is clear evidence that this is not the case in marine fishes and mammals. Hence, reproductive monogamy does not appear to have a single overriding explanation, but is more taxon specific. Genetic compatibility is a promising avenue for future work likely to improve our understanding of monogamy and other mating patterns. I also discuss eight important consequences of reproductive monogamy: (i) parentage, (ii) parental care, (iii) eusociality and altruism, (iv) infanticide, (v) effective population size, (vi) mate choice before mating, (vii) sexual selection, and (viii) sexual conflict. Of these, eusociality and infanticide have been subject to debate, briefly summarised herein. A common expectation is that monogamy leads to little sexual conflict and no or little sexual selection. However, as reviewed here, sexual selection can be substantial under mutual monogamy, and both sexes can be subject to such selection. Under long‐term mutual monogamy, mate quality is obviously more important than mate numbers, which in turn affects the need for pre‐mating mate choice. Overall, I conclude that, despite much research on genetic mating patterns, reproductive monogamy is still surprisingly poorly understood and further experimental and comparative work is needed. This review identifies several areas in need of more data and also proposes new hypotheses to test.
