Paternity analysis in the golden egg bug using AFLPs: do the males preferentially accept their true genetic offspring? (original) (raw)
Related papers
Evolution, 2003
Theoretical models predict how paternal effort should vary depending on confidence of paternity and on the trade-offs between present and future reproduction. In this study we examine patterns of sperm precedence in Phyllomorpha laciniata and how confidence of paternity influences the willingness of males to carry eggs. Female golden egg bugs show a flexible pattern of oviposition behavior, which results in some eggs being carried by adults (mainly males) and some being laid on plants, where mortality rates are very high. Adults are more vulnerable to predators when carrying eggs; thus, it has been suggested that males should only accept eggs if there are chances that at least some of the eggs will be their true genetic offspring. We determined the confidence of paternity for naturally occurring individuals and its variation with the time. Paternity of eggs fertilized by the last males to mate with females previously mated in the field has been determined using amplified fragment length polymorphisms (AFLPs). The exclusion probability was 98%, showing that AFLP markers are suitable for paternity assignment. Sperm mixing seems the most likely mechanism of sperm competition, because the last male to copulate with field females sires an average of 43% of the eggs laid during the next five days. More importantly, the proportion of eggs sired does not change significantly during that period. We argue that intermediate levels of paternity can select for paternal care in this system because: (1) benefits of care in terms of offspring survival are very high; (2) males have nothing to gain from decreasing their parental effort in a given reproductive event because sperm mixing makes it difficult for males to reach high paternity levels and males are left with no cues to assess paternity; (3) males cannot chose to care for their offspring exclusively because they can neither discriminate their own eggs, nor can they predict when their own eggs will be produced; and (4) males suffer no loss of further matings with other females when they carry eggs. Thus, our findings do not support the traditional view that paternal investment is expected to arise only in species where confidence of paternity is high. The results suggest that females maximize the chances that several males will accept eggs at different times by promoting a mechanism of sperm mixing that ensures that all males that have copulated with a female have some chance of fathering offspring, that this probability remains constant with time, and that males have no cues as to when their own offspring will be produced.
Journal of Insect Behavior - J INSECT BEHAV, 2000
Females of the golden egg bug, Phyllomorpha laciniata, lay eggs on the backs of conspecifics. Male response to female oviposition attempts is either passive or resistant. Passive males remain still during oviposition, while resistant males move repeatedly and thereby delay or avoid being encumbered. We investigated how previous mating experience affected male acceptance of eggs. Males from two Spanish populations, from Andalusia and Catalonia, were allowed to mate with single females repeatedly. These experimental pairs were then presented with either a single, nonmating male or a pair in copula. We expected mating partners to resist oviposition attempts less strongly than nonmating males but no differences were detected. However, there was a significant difference in behavior exhibited by males from the two populations; males from Catalonia were relatively passive but males from Andalusia routinely resisted encumbrance. Predation pressure and the availability of receptive females m...
Female egg dumping and the effect of sex ratio on male egg carrying in a coreid bug
Behavioral Ecology, 1997
PhyUomorpha lacmiata Vill (Heteroptera, Coreidae) is unique among teiieauial infects in that females ghie eggi on the back* of other conspecifics. Egg carrying by P. lacmiata males has previously been considered as paternal care. We explored female oviposidon with respect to previous mating experience of females and tested whether sex ratio affects male egg-carrying. The hypothesis that male egg-carrying is a form of paternal care predicts that a male should always accept eggs after mating with a female. However, if male egg-carrying is a form of postcopulatory mate guarding rather than paternal care, egg carrying should increase in die presence of other males. When two couples were placed together, females laid eggs on the backs of all individuals enclosed, including the backs of other females. However, when a female was accompanied by 2 males, 22 out of 26 females oviposited on their mating partner. Thus, sexual compeddon rather than paternity alone, affects a male's eagerness to carry eggs. However, even if males sometimes carry their own eggs, females lay eggs on the backs of all conspecifics they can easily acquire. Thus, egg carrying in P. lacmiata is partially voluntary and partially die result of female egg dumping. Ktj words: Coreidae, egg carrying, Heteroptera mate guarding, paternal care, PhyUomorpha lacmiata, sex ratio. (1997)1 I nsects face high offspring mortality due to predation because eggs are often left undefended. A female can decrease offspring mortality by laying eggs in a safe place or by defending them (Tallamy, 1984; Tallamy and Wood, 1986). Egg defense is more common among females (Tallamy, 1984, and only rarely are eggs defended exclusively by males
Conflict over male parentage in social insects
2004
Mutual policing is an important mechanism that maintains social harmony in group-living organisms by suppressing the selfish behavior of individuals. In social insects, workers police one another (worker-policing) by preventing individual workers from laying eggs that would otherwise develop into males. Within the framework of Hamilton's rule there are two explanations for worker-policing behavior. First, if worker reproduction is cost-free, worker-policing should occur only where workers are more closely related to queen-than to worker-produced male eggs (relatedness hypothesis). Second, if there are substantial costs to unchecked worker reproduction, worker-policing may occur to counteract these costs and increase colony efficiency (efficiency hypothesis). The first explanation predicts that patterns of the parentage of males (male parentage) are associated with relatedness, whereas the latter does not. We have investigated how male parentage varies with colony kin structure and colony size in 50 species of ants, bees, and wasps in a phylogenetically controlled comparative analysis. Our survey revealed that queens produced the majority of males in most of the species and that workers produced more than half of the males in less than 10% of species. Moreover, we show that male parentage does not vary with relatedness as predicted by the relatedness hypothesis. This indicates that intra-and interspecific variation in male parentage cannot be accounted for by the relatedness hypothesis alone and that increased colony efficiency is an important factor responsible for the evolution of workerpolicing. Our study reveals greater harmony and more complex regulation of reproduction in social insect colonies than that expected from simple theoretical expectations based on relatedness only.
Determinants of paternity in a butterfly
Proceedings of the Royal Society B: Biological Sciences, 1998
Success in sperm competition is of fundamental importance to males, yet little is known about what factors determine paternity. Theory predicts that males producing high sperm numbers have an advantage in sperm competition. Large spermatophore size (the sperm containing package) also correlates with paternity in some species, but the relative importance of spermatophore size and sperm numbers has remained unexplored. Males of the small white butter£y, Pieris rapae (Lepidoptera: Pieridae), produce large nutritious spermatophores on their ¢rst mating. On their second mating, spermatophores are only about half the size of the ¢rst, but with almost twice the sperm number. We manipulated male mating history to examine the e¡ect of spermatophore size and sperm numbers on male fertilization success. Overall, paternity shows either ¢rst male or, more frequently, second male sperm precedence. Previously mated males have signi¢cantly higher fertilization success in competition with males mating for the ¢rst time, strongly suggesting that high sperm number is advantageous in sperm competition. Male size also a¡ects paternity with relatively larger males having higher fertilization success. This may indicate that spermatophore size in£uences paternity, because in virgin males spermatophore size correlates with male size. The paternity of an individual male is also inversely correlated with the mass of his spermatophore remains dissected out of the female. This suggests that females may in£uence paternity by a¡ecting the rate of spermatophore drainage. Although the possibility of female postcopulatory choice remains to be explored, these results clearly show that males maximize their fertilization success by increasing the number of sperm in their second mating.
Evolution, 2012
Female multiple mating (polyandry) has nevertheless evolved several times in the social Hymenoptera (ants, bees, and wasps), and a substantial amount of work has been conducted to understand its costs and benefits. Relatedness and inclusive fitness benefits are, however, not only influenced by queen mating frequency but also by paternity skew, which is a quantitative measure of paternity biases among the offspring of polyandrous females. We performed a large-scale phylogenetic analysis of paternity skew across polyandrous social Hymenoptera. We found a general and significant negative association between paternity frequency and paternity skew. High paternity skew, which increases relatedness among colony members and thus maximizes inclusive fitness gains, characterized species with low paternity frequency. However, species with highly polyandrous queens had low paternity skew, with paternity equalized among potential sires. Equal paternity shares among fathers are expected to maximize fitness benefits derived from genetic diversity among offspring. We discuss the potential for postcopulatory sexual selection to influence patterns of paternity in social insects, and suggest that sexual selection may have played a key, yet overlooked role in social evolution.
Paternity assurance by ?helpful? males: adaptations to sperm competition in burying beetles
Behavioral Ecology and Sociobiology, 1989
Male burying beetles invest parentally by participating in the burial of a carcass and in provisioning and guarding the larvae that come to the carcass. Since most of the females arriving at a carcass have stored fertile sperm within their spermathecae, sperm transferred by such "helpful" males must compete with other males' ejaculates for the fertilization of the female's eggs. We showed that these males are able to achieve a high level of paternity (mean=92%). The mechanism they employ is a repeat-mating tactic, i.e., the female is mated very frequently shortly before and during oviposition. Repeated matings are essential for a high reliability of paternity, since single copulations result in the fertilization of only a very small proportion of the female's eggs.
Paternity following multiple mating in ladybird Harmonia axyridis
BioControl, 2017
We investigated factors which may determine realised paternity following multiple mating in a promiscuous ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), namely the mating order and ability of males of different morphs to fertilize females. In experiments using males of two colour morphs, we found that the first male had a reproductive advantage over the second male (sperm precedence P2 = 0.38). Males of the melanic morph spectabilis had a reproductive advantage over males of the semi-melanic morph axyridis (P2 = 0.35). Analysis of paternity using microsatellites applied to young larvae, which avoids possible differential mortality of progeny, confirmed the precedence of the first male and higher paternity rate of colour morphs that are more frequent in the wild. Hatchability of eggs increased from 65% after the first mating to 85% after the second mating delayed by five days. Average duration of mating was 157 min and did not differ between the first and second mating and between the colour morphs of males.
Entomological Science, 2011
The giant water bug Appasus major exhibits a peculiar reproductive behavior where females lay eggs on the backs of males. A male and female pair performs frequent repeat copulations during the oviposition behavior, and the male carries the deposited eggs until hatching. Such characteristic behaviors predict that the eggs are fertilized by the brooding males. If males carry eggs of other unrelated males, the egg carrying will drastically decrease the fitness of the carriers. In this study, we examined genetic relationships between the 489 eggs and nine males carrying them collected from the field, using microsatellite DNA markers. We revealed that in total, 28.4% of the eggs were of other male origin. This is the first report of frequent brood parasitism in an aquatic egg-carrying hemipteran insect. The brood parasitism is adaptive for the females probably because it enables them to increase the chance of oviposition, or it can equalize motility risk of the eggs of each mate.