Ebook Animal behaviour - An evolutionary perspective: Part 2

Chia sẻ: _ _ | Ngày: | Loại File: PDF | Số trang:206

Thêm vào BST

Báo xấu

2
lượt xem 0
download

Download Vui lòng tải xuống để xem tài liệu đầy đủ

Part 2 book "Animal behaviour - An evolutionary perspective" by author Peter M. Kappeler includes content: Intersexual selection - how females choose, parental care, development and control of behaviour, social systems, social structure.

Chủ đề:

Bình luận(0) Đăng nhập để gửi bình luận!

Lưu

Nội dung Text: Ebook Animal behaviour - An evolutionary perspective: Part 2

199 10 Intersexual Selection: How Females Choose Swans mate for life – so, the right mate must be well chosen. (© JuliaMimages/Pixabay) © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 P. M. Kappeler, Animal Behaviour, https://doi.org/10.1007/978-3-030-82879-0_10
Contents 10.1 S pecies Recognition – 201 10.2 I ncest Avoidance – 204 10.3 M echanisms of Mate Choice – 209 10.3.1 reference Functions – 209 P 10.3.2 ampling Tactics – 211 S 10.3.3 C hoosiness – 214 10.4 irect Benefits of Mate Choice – 214 D 10.5 I ndirect Benefits of Mate Choice – 217 10.5.1 exy Sons Through the Fisher Process – 218 S 10.5.2 B etter Offspring Through Good Genes – 221 10.5.3 G enetic Compatibility – 226 10.6 olyandry – 227 P 10.7 C ompetition Among Females – 231 10.8 S ummary – 235 L iterature – 235
10.1 · Species Recognition 201 10 In contrast to males, females cannot increase embryonic development and thus lose valu- their reproductive success by engaging in able time and opportunity to reproduce suc- additional matings. Instead, they can improve cessfully. Females can therefore be expected the quality and survival chances of their off- to have evolved mechanisms for recognising spring through increased maternal care and males that enable them to produce viable and the choice of an appropriate mate. When fertile offspring. Intersexual selection can choosing a mate, members of closely related therefore be an important mechanism in either species and conspecific kin should be avoided. preventing or facilitating speciation in diver- Through appropriate choice, females can gent populations (Mendelson and Shaw 2012). derive direct benefits for themselves or indi- Differentiation of one species into two rect benefits for their young, and their choice daughter species can be achieved through can be mediated by a variety of mechanisms. intersexual selection if a simultaneous change There are also adaptive reasons why females in partner preferences of females and second- seem to mate indiscriminately with several ary sexual traits of males within a population males, and reproductive competition between leads to prezygotic isolation. Prezygotic iso- females appears to be more widespread than lation in the form of partner discrimination described by classical sex roles. Intersexual is the main cause of reproductive isolation selection is therefore a driving evolutionary among allopatric or secondarily sympatric force in speciation and the evolution of orna- populations. Since sexual selection in this ments, as well as sex differences within a wide case directly affects traits involved in mate diversity of traits. identification, this process can quickly lead to divergence among populations, regardless of environmental conditions. In particular, dif- 10.1 Species Recognition ferences among allopatric populations can be enhanced, but sympatric speciation can also The first important decision that females that occur based on this mechanism. are ready to reproduce have to make concerns Cichlids in African lakes are a particu- the identification of a male of their own spe- larly suitable group for the study of speciation cies. Although species are defined by the bio- mechanisms, because hundreds of species logical species concept as closed reproductive have evolved there over the last few millennia, units due to reproductive isolation, matings of some of which are ecologically and morpho- members of closely related species do occur logically very similar. In the genus Pundamilia, (Baker and Bradley 2006). When prezygotic there are, for example, two sister species (P. isolation mechanisms, including female mate pundamilia and P. nyerery), whose females are choice, fail and heterospecific matings take very difficult to distinguish because they are place, these often lead to disturbances in early similar in size and cryptically coloured. Male embryonic development and to the death of P. pundamilia are blueish in colour, whereas the developing embryos. Sometimes, however, P. nyerery males have a striking red-ellow y hybridisation does occur, with the resulting pattern. Maan et al. (2004) showed that P. bastards typically showing increased vitality, nyerery females are ultimately responsible for but reduced fertility. In the vast majority of the red colour of their males and thus for the cases, the heterogamous sex is more affected differentiation of these two species (7 Box by these disadvantages (Haldane’s rule). These 10.1). This sensory drive as the basis for sym- postzygotic isolation mechanisms also gener- patric population differentiation has also led ate fitness costs that mainly affect females; to ecological and genetic separation and thus they lose their investment in oocytes and to speciation (Seehausen et al. 2008).
202 Chapter 10 · Intersexual Selection: How Females Choose Box 10.1 Female choice and speciation whether P. nyerery evolved because their 55 Question: Did female preferences contrib- females prefer red males. ute to speciation in cichlids? 55 Method: Single captive P. nyerery females 55 Background: The females of two species were presented with two differently red (Pundamilia pundamilia and P. nyerery) look coloured males in separate aquariums. The very similar, whereas the males are clearly approach reaction of the females to differ- different (P. pundamilia: blue; P. nyerery: ent components of male courtship behav- red). Since the original colour of Pundamilia iour was quantified. males is blue, the question arises as to 0.6 Female reaction * * High redscore 0.4 ** 0.2 Low redscore 0 Lateral Quiver Lead display swim 10 55 Result: Females showed a significant prefer- (Maan et al. 2004; Pundamilia: Martine Maan). ence* for the more intense red colour of *Measured as swimming towards males two males, which did not differ in size or that exhibited a “lateral display”, “shake” or intensity of courtship behaviour. “swim forward”. 55 Conclusion: Female P. nyerery have a strong preference for red males. This probably accidental preference has led to a rapid sep- aration into two species. When two allopatric populations meet ulations than in homospecific matings (Giesen again after a long separation before spe- et al. 2017). Thus, if the males of two species ciation is complete, it is possible that rein- are very similar in appearance, female mate forcement serves to establish reproductive choice may lead to very elaborate courtship isolation and complete the speciation pro- behaviour, presumably so that females can cess. Reinforcement may result from tenden- carefully evaluate a maximum amount of cies towards assortative mating, i.e. females information to avoid mating with a foreign prefer similar phenotypes for reproduction. male. Studies on two species of dung fly (Sepsis When hybridisation between different spe- spp.) confirmed the importance of female cies occurs, its fitness costs strengthen selective mate selection in this process. In experiments, forces that drive differentiation of the affected the latency to mate was greater when the two populations, leading to reproductive charac- partners belonged to different species. Males ter displacement (Higgie et al. 2000). This is did not differ in how often they initiated mat- defined by the fact that closely related sympat- ing, whereas females “shook” longer before ric species differ more in the mechanisms of agreeing to heterospecific mating. These sex mate recognition than allopatric populations, differences were much more pronounced in with natural and sexual selection interacting matings between members of sympatric pop- in the expression of mate recognition mecha-
10.1 · Species Recognition 203 10 nisms. For example, the calls of male North times for hours. In this situation, females can American chorus frogs (Pseudacris spp.) in the directly compare not only the species affilia- overlapping area of their respective geograph- tion of a male but also phenotypic correlates ical ranges differ much more in structural of their quality. The acoustic structure of the features than in areas where only one species sounds of different species, as well as the pos- occurs at a time (Lemmon 2009). Hybrids of tures of the males during sound production, the two species show a 44% reduction in fit- is complex and species specific (. Fig. 10.2). ness, with intersexual selection against hybrid For the Hawaiian cricket genus Laupala, males being four times greater than the losses which has the highest known speciation rate in male fertility assessed by natural selection among arthropods, some species can only be (Lemmon and Lemmon 2010). The reproduc- distinguished by their songs (Mendelson and tive character shift is thus increased by rein- Shaw 2012), and two species of wood warbler forcement, i.e. females have trait preferences (Vermivora spp.), which have been hybridising that greatly reduce the probability of hetero- for a long time, differ only in six small gene specific mating (. Fig. 10.1). regions that are responsible for the expression Also, in crickets and grasshoppers, the of the different plumage colours (Toews et al. “songs” produced by males through stridula- 2016). tion with their hind legs and wings play the If prezygotic isolation mechanisms fail, most important role in reproductive isolation fertilisation can be prevented at the last of sympatric species. In the field grasshop- moment by the fact that the genitalia do not per (Chorthippus albomarginatus), females fit mechanically. Especially in arthropods, are surrounded by several “singing” males, male reproductive organs are shaped in a which produce their courtship sounds, some- complex way, so that they often represent the Tennessee P. nigrita Florida Hybrid 6 10 14 18 22 25 30 34 Pulse rate (14°C) P. nigrita F1 Hybrid P. feriarum P . feriarum Geographic overlap Reproductive character Acoustic signals displacement .. Fig. 10.1 Two species of chorus frog overlap in their their call structure differs more clearly from that of their geographical ranges. In this area, the males of the north- sympatric sister species than the calls of the two allopat- ern species have a call rate that is more than three times ric populations. (After Lemmon and Lemmon 2010; higher than in the rest of their distribution range and chorus frogs: Emily Claire Lemmon)
204 Chapter 10 · Intersexual Selection: How Females Choose Species A Species B .. Fig. 10.2 Species identification and hybridisation the postures adopted during their production. (Vedenina along a hybrid zone. In grasshoppers of the genus Chor- and von Helversen 2003; grasshopper: Andreas thippus, hybridisations occur between two species (A Stumpner) 10 and B), whose males differ in their courtship songs and most reliable feature for taxonomists – and 10.2 Incest Avoidance probably also for the respective females – for species identification (. Fig. 10.3). Females should also be careful to discriminate According to the key and lock hypothesis, against a second group of males during mat- complex genitalia act as a mechanism to ing, in addition to heterospecific males: close prevent hybridisation, since there is either relatives. Mating between relatives should be no exact fit, and thus no sperm transfer, or avoided, as the accumulation of homozygous the resulting hybrid males have poorly fitting alleles can lead to inbreeding depression. This genitalia and therefore have reduced repro- can lead to a reduction in birth weight, sur- ductive success (Langerhans et al. 2016). vival and reproduction rates, as well as resis- According to a non-exclusive alternative tance to diseases or ecological stressors, the hypothesis, selection affects male genitalia costs of which are also largely borne by the by evaluating their reproductive success, females. Inhibition to reproduce with related i.e. after insemination. According to this males alone may be associated with costs. For hypothesis, appropriately decorated penises example, female striped mice (Rhabdomys stimulate the female genital tract and thus pumilio) raised experimentally with their influence cryptic female choice (7 Sect. fathers showed delayed sexual maturation 10.3), i.e. processes inside the female genital and reduced reproductive success compared tract that determine which sperm are selected to controls who grew up with foreign males for fertilisation after multiple matings. In (Pillay 2002). Females should therefore have fact, genital anatomy is much more variable developed mechanisms for identifying and in those insect species in which females mate rejecting males with high genetic similarity to multiple times (Arnqvist 1998). reduce the risk of incestuous mating. Indeed,
10.2 · Incest Avoidance 205 10 Population genetic studies (e.g. on black grouse, Tetrao tetrix, Lebigre et al. 2010) have shown that natal dispersal alone effectively reduces the risk of inbreeding. In the case of limited dispersal possibilities, incest avoid- ance can nevertheless have a pronounced effect on the reproductive behaviour of females. In mountain brushtail possums (Trichosurus cunninghami), a small nocturnal marsupial, relatives remain near their natal area, but inbreeding does not occur due to female choice (Blyton et al. 2016). In cooperatively breeding birds (Sect. 7 11.4), sexually mature offspring remain with their parents and help them to raise the next brood. In such groups, if the breeding male dies, the female finds herself in the territory of her eldest son. In this situation, most females disperse, thereby avoiding mating with their sons (Cockburn et al. 2003). A similar problem arises for females whose choice of unrelated mates is limited. In several species of Arctic sandpiper (Calidris mauri, Actitis hypoleuca and Charadrius alexandrinus . Fig. 10.4), matings between relatives occur regularly for reasons that are not well under- stood. Both sexes participate in incubation, but males invest considerably more. Foreign offspring in a nest can therefore be due to mat- ings of the female with a second male or origi- .. Fig. 10.3 Male genitalia of numerous insects are provided with complex appendages and outgrowths (here, in the cowpea weevil, Callosobruchus maculatus). Two evolutionary hypotheses explain this diversity of form; one of them postulates a function in species recog- nition. (Andrew Syred) mating with related males is often much rarer than would be expected from random mating; for example, in silver gulls (Larus novaehol- landiae), more than 12,000 observed mating events did not involve a single one between relatives (Alho et al. 2012). The easiest way to reduce the risk of .. Fig. 10.4 For western sandpipers (Calidris mauri), inbreeding is to disperse away from the natal mating between related animals occurs regularly, area. In this case, it is sufficient and effective if although they can determine genetic similarity. (Alan the members of one sex disperse (7 Sect. 13.2). D. Wilson, 7 www.naturespicsonline.com)
206 Chapter 10 · Intersexual Selection: How Females Choose nate from eggs that foreign females have laid and dispersal are not strictly linked and when in the common nest that were then incubated there is a difference between the sexes in these by the male. A comparison of the frequency traits. In polygynous mammals, in which males of offspring not originating from the social are in a reproductive position longer than parents with the genetic similarity between females need to reach sexual maturity, females males and females showed that the proportion exceptionally disperse from their birth group of foreign offspring increased with increasing (Clutton-Brock 1989), ostensibly to avoid mat- genetic similarity between the social parents ing with their fathers. (Blomqvist et al. 2002). In this case, “cheating” Besides precopulatory mechanisms of can be interpreted as an adaptation to avoid inbreeding avoidance, females also seem to the genetic disadvantages of mating with rela- be able to selectively discriminate against tives. These birds can thus apparently deter- sperm of related males after multiple matings mine their genetic similarity to conspecifics, (. Fig. 10.5). In one experiment, female two- but nevertheless sometimes mate with relatives. spotted crickets (Gryllus bimaculatus) either Since reproductive success in some species mated with two brothers, two unrelated males is strongly skewed in favour of dominant males or one related and one unrelated male each, and (7 Sect. 9.3), it may happen that the offspring the number of hatched offspring was counted of different females in the same age cohort afterwards (Tregenza and Wedell 2002). After have the same father. In this case, mating mating with two brothers, significantly fewer between individuals that are related through offspring hatched from the fertilised eggs than the paternal line should be avoided. In savan- in the other combinations. Since reproductive nah baboons, it was observed that sexual inter- success after mating with one relative and one 10 actions between siblings with the same father unrelated (regardless of their mating order) indeed occurred less frequently than between did not differ from hatching success after mat- unrelated animals (Alberts 1999). This prob- ing with two foreign males, females must have lem therefore occurs when sexual maturity selectively preferred the sperm of the foreign 0.6 0.5 % Hatched young 0.4 0.3 B+B N-K + N-K B + N-K N-K + B Female mating options .. Fig. 10.5 Polyandry as a possible mechanism of they mate with brothers (B) or unrelated males (U) in incest avoidance. When female crickets are mated with other combinations. (After Tregenza and Wedell 2002; two males, significantly fewer offspring hatch from eggs crickets: Ulrike Walbaum) fertilised in mating with two brothers (B + B) than when
10.2 · Incest Avoidance 207 10 males. If this cryptic post-copulatory mecha- This is possible if relatives are located only nism is widespread, polyandric matings of in certain places with very high probabilities. females can also be interpreted as a mecha- For example, some birds consider and treat nism to avoid inbreeding. all young in their nest as offspring, but ignore In cases when females try to avoid mat- their own young that are only slightly out- ing with related males, they require proximate side the nest. This mechanism is exploited by mechanisms of kin recognition. Three compo- brood parasites (e.g. common cuckoo, Cuculus nents are necessary to recognise kin: canorus), since the hosts also incubate these . Existence of a phenotypic signal encoding 1 foreign eggs and treat the young that hatch genetic similarity. from them like their own. However, there is no 2. Perception. known example of mate discrimination based . Matching of this signal with an internal 3 on this mechanism. template, i.e. a mostly learned internal rep- A second form of kin recognition is based resentation of an expected value that is on phenotype matching. It is thought that indi- formed on the basis of interactions with viduals have an internal kinship template that external referents (Penn and Frommen they match with the observed phenotype. This 2010). In some species, such a template is mechanism is postulated when animals recog- also formed under the influence of its per- nise relatives or distinguish between known but sonal traits; the notion of how relatives differently closely related individuals without smell, for example, is formed by an indi- prior contact (7 Box 10.2). The actual recog- vidual’s own smell. nition can be based on a wide range of sig- nals. Many invertebrates carry colony-specific Discrimination among conspecifics with dif- odours on the body surface that are passed on ferent degrees of kinship also plays an impor- through direct body contact and have signifi- tant role in many aspects of social behaviour. cance within this context (Linsenmair 1987). Many studies of the mechanisms of kin rec- In golden hamsters, recognition of relatives ognition have therefore been conducted in the is also achieved via olfactory signals that are context of other questions and not in the con- compared with their own odour (Mateo and text of mate choice. Johnston 2000). In primates, there is evidence Currently, four mechanisms of kin recog- that visual features of the face or structural nition are recognised. First, the simplest way features of acoustic signals are more similar of categorising conspecifics into relatives and between relatives than between non-relatives non-relatives is to use spatial information. (Rendall 2004). Box 10.2 Kin recognition and incest avoidance great potential for inbreeding. Females 55 Question: Do female cockroaches (Blattella mate only once. germanica) discriminate against related 55 Method: In breeding experiments, five cate- males and, if so, how do they recognise gories of adult were created, which differed them? in their degree of familiarity and kinship 55 Background: Cockroaches live in aggrega- (siblings (r = 0.5), own (0 ≤ r
208 Chapter 10 · Intersexual Selection: How Females Choose 100 I 100 100 II III 80 Familiarity and 80 Familiarity 80 Familiarity Mating rate (%) kinship 60 60 60 40 40 40 20 20 20 0 0 0 Male category Male category Male category 100 Familiar brother 100 IV V Unfamiliar brother 80 Kinship Familiar strain member 80 Kinship Mating rate (%) Unfamiliar strain member 60 60 Unfamiliar stranger 40 40 20 20 0 0 Male category Male category 55 Result: Females preferred foreign strain 55 Conclusion: Female cockroaches recognise 10 members over known siblings (I). Both and discriminate against closely related between siblings and strangers, females did males. Recognition is not based on famil- not discriminate against familiar males (II, iarity, but on a phenotype matching of III). Unknown strain members were pre- genetic information. ferred over unknown siblings (IV), but not over unfamiliar non-kin (V). Body size had (Lihoreau et al. 2007; cockroaches: no influence on male mating success. M. Lihoreau). A third mechanism of kin recognition about the MHC genotype of an individual consists of direct recognition of the degree to conspecifics, such as females choosing a of relatedness by means of a correlate that is mate. MHC-dependent odour information as reliable as possible. Since genetic similar- can indeed be used by rodents to determine ity itself cannot be detected directly, the gene genetic similarity (Leinders-Zufall et al. product should be as immediate as possible. 2004). The genes of the major histocompatibility An alternative mechanism for identifying complex (MHC) are, in principle, suitable for relatives has been discovered in house mice, this type of kin recognition. They produce the females of which often raise their offspring different molecules that attach to foreign together with close relatives (Sect. 7 11.4). and own peptides inside a cell and present In experiments, mice were able to recognise them to T-lymphocytes on the cell surface unfamiliar sisters with identical genotypes for for differentiation. The more MHC alleles genes of the major urinary peptide (MUP) an individual has, the larger its spectrum of region and formed a joint nest with them. The MHC molecules and the larger the spectrum genes of the MUP region are inherited inde- of parasite peptides that can be presented to pendently of the MHC genes and their pro- the T-ymphocytes. These presented peptides l teins are found in high concentrations in urine therefore represent a kind of blueprint of the (Green et al. 2015). So far, however, there is MHC molecules and may signal information little empirical evidence for a specific use of
10.3 · Mechanisms of Mate Choice 209 10 information in both the MHC and MUP for from the question of what criteria they use to incest avoidance (Ferkin 2018). make their choice. There is no uniform answer Since kin recognition per se is not possible, to this question, since female mate choice in with, at best, the similarity of alleles on sev- different species takes place under very dif- eral gene loci possibly being determined via ferent conditions. Females can often choose their products, individuals of many species among courting males, as males generally rely on a simpler mechanism that works quite invest more in mate searching. In species with reliably under natural conditions: familiarity. lek mating systems, females come to court- It distinguishes strangers from individuals ship arenas where they can directly compare with whom one grew up or whom one got to several potential mates at the same time and know as kin during early individual develop- mate with the selected male(s). In other spe- ment. This familiarity is often acquired and cies, males defend individual territories and established during a sensitive phase, which is are visited there by females ready to mate. completed before reaching sexual maturity, Still other species live in permanently bisex- in a process similar to imprinting. However, ual groups, i.e. potential mates live together it is not clear which signals are proximately all year round and the females know exactly involved or of particular importance. This which males are available. What behavioural mechanism can be elegantly demonstrated tactics do females use to search, compare and experimentally with transplantation experi- decide in these different situations? Several ments. Young animals raised with strangers independent factors interact in this context prefer them later as social partners and avoid (Neelon et al. 2019): preference functions, them as mates, compared to siblings who grew sampling tactics and choosiness restrict the up separately. This mechanism also prevents number of potential partners, and preference mating between parents and their offspring. for certain expressions of relevant male traits, In striped mice, daughters raised with either together with social factors, determines the their biological father or experimental step- actual choice of a mate (. Fig. 10.6). father exhibit the same delays and deficits in reproductive behaviour (Pillay 2002). Young females that were exchanged between breed- 10.3.1 Preference Functions ing pairs shortly after birth were, after wean- A preference function, which is used to rank ing, reunited either with their biological father or with the male they grew up with. Of every potential mates, describes the relationship 15 females, 9 reproduced with the biological between the expression of a male trait and the father, who was unfamiliar to them, whereas corresponding female reaction. Accordingly, only one female reproduced with the familiar depending on the phenotypic variation among stepfather. The recognition and discrimina- males, females may align their preferences tion of kin as potential mating partners are with a threshold, categorise males, adapt them therefore clearly not based on a phenotype linearly to the variation in the male trait, or match, but on the degree of familiarity. For either prefer or reject average male pheno- cockroaches, however, it was shown that types (. Fig. 10.7). familiarity does not play a role in the discrimi-In this context, sensory processes and nation of relatives (7 Box 10.2). innate templates play a role. There are both innate preferences for traits that identify mem- bers of one’s own species and female prefer- 10.3 echanisms of Mate Choice M ences for specific traits of males of the same species. Since the traits in question are often Mate choice occurs whenever the effects ornaments, their characteristics are evaluated of traits developed in one sex lead to non- by the females. In this context, either an exist- random mating with members of the oppo- ing perceptual bias influences the decision of site sex. The question of how females select females or any such biases are exploited by the their mating partners must be distinguished males (Ryan and Cummings 2013). For exam-
210 Chapter 10 · Intersexual Selection: How Females Choose Physiological Innate tendency constraints Preference function Sampling tactic Selectivity Mating preference Social constraints Mating competition Mate choice (operational sex ratio) Sexual selection .. Fig. 10.6 Determinants of mating preferences. Mat- These components are interlinked with other aspects of ing preferences are influenced by a preference function, sexual selection and ultimately determine mate choice a certain sampling tactic and the choosiness of females. ple, if a female sees particularly well within a Physalaemus have a preference for a two- certain wavelength range or hears particularly syllabled advertising call of males from 10 well within a certain frequency range, males that serve these sensory sensitivities with their closely related species, even if their own males are monosyllabic (Ryan and Rand ornaments are more likely to be preferred by 1993). In swordtails (Xiphophorus spp.), females. This can quickly lead to an evolu- females have a preference for a sword on tionary coupling of preference and trait, so the male anal fin, even if the males of their that males with intensive or even exaggerated own species do not have one (Basolo 1990). ornamentation are preferred simply because When female swordtails are presented with of the higher signal value; they engage in a an attractive male, genes are activated in the sensory exploitation of the females. It is not neurons of a certain brain area and switched uncommon in this context for males to trans- off in the presence of an unattractive male mit and for females to evaluate information (Cummings et al. 2008). In African widow- from several sensory modalities simultane- birds (Euplectes spp.), not only do females ously (Simmons et al. 2013). of long-tailed species have a preference for Several comparative studies have shown males with particularly long (or experimen- that the female preference must have evolved tally extended) tail feathers (. Fig. 10.8), before the corresponding male trait, i.e. but females of short-tailed species also have females have pre-existing preferences. For a preference for species-atypical long tails example, females in the dwarf frog genus (Pryke and Andersson 2002). Threshold Categorical Linear Stabilising Disruptive a b c d e .. Fig. 10.7 Female preference function can take different forms in terms of male phenotypic variability (x-axis). (After Edward 2015)
10.3 · Mechanisms of Mate Choice 211 10 .. Fig. 10.8 The long tail feathers of the African widowbird (Euplectes progne) have probably been selected by cor- responding female preferences. (© Richard Du Toit/Minden Pictures/picture alliance) In addition to innate preferences, there are 10.3.2 Sampling Tactics also those that are shaped during a sensitive phase by sexual imprinting. Imprinting is the Since there is individual variation among term used to describe learning processes that males, females should not be indifferent take place once during a pre-programmed about with whom they mate. In fact, selection sensitive phase in the course of individ- should reward females who find the highest ual development and is often irreversible quality males at the lowest possible cost. In (Immelmann 1972). With sexual imprinting, order to understand different sampling tactics the fixation of a preference takes place in two in the context of female choice, it is therefore steps. The preference for species-specific char- especially necessary to consider mate qual- acteristics (e.g. the father’s song) is acquired ity and the costs of sampling (Gibson and during an early acquisition phase, consoli- Langen 1996). dated in a later phase and only then linked With regard to the quality of potential to sexual behaviour. The effects of sexual mates, there are three possibilities. Firstly, imprinting can be impressively demonstrated there can be absolute differences in quality with translocation experiments. If, for exam- between males, so there is one best male that ple, eggs of great tits are incubated and reared all females should find and prefer. Secondly, by blue tits, these individuals have greater dif- there can be an individual best male for each ficulty in successfully mating and reproduc- female, so that different females will look ing with a member of their own species than for different mates. Finally, it is also possi- great tits reared by great tits (Slagsvold et al. ble that females have only certain minimum 2002). The reverse experiment with blue tits requirements that are met by several males in even leads to successful mating between the their population. The specific quality traits two species; the imprinting effects thus domi- that females of different species evaluate nate other mechanisms of species recogni- differ among species; they can select males tion. Partner preferences at the species level according to direct advantages, genetic traits can thus be strongly canalised by both innate or their suitability as partners in parental and acquired factors. care.
212 Chapter 10 · Intersexual Selection: How Females Choose Studies on numerous species have shown best of N from this sample. Secondly, females that female choice is never unanimous, i.e. could also visit several males until they meet not all females mate with only one particular one whose quality exceeds a certain threshold. male (. Fig. 10.9). This could potentially be Since females, in reality, often do not meet explained by one of the following facts: males by chance, a third tactic seems to be . Dominant females monopolise the best 1 common, which is based on sequential hier- male for themselves. archical reduction. According to this notion, . These best males, if they exist, do not have 2 females concentrate on a subgroup of males enough time, energy and sperm to fertilise due to individual preferences or remotely all females. available information, from which males are . Some males fake high quality. 3 then selected according to additional criteria . Females do not restrict themselves to one 4 (Mays and Hill 2004). male for adaptive reasons, but mate with Which of these tactics is more advanta- several males. geous in a specific case depends above all on search costs. In addition to the energetic costs Furthermore, since it is impossible for females of the search, predation risk, running out of to meet and evaluate all males of a popula- time (which is significant for species that can tion, i.e. they lack perfect information, theo- only reproduce within a short time window retical models of active mate choice do not for ecological reasons), the risk of being sexu- assume that females are searching for the ally harassed by males and the risk of losing absolutely best male. an acceptable partner to another female may Instead, it is assumed that females meet all contribute to these costs. As costs increase, 10 potential mates sequentially, with males vary- females should become less choosy and should ing randomly in quality, and that females therefore visit fewer males or lower their qual- can correctly detect these quality differences. ity threshold, as has been shown for female Under these assumptions, three tactics are pos- three-spined sticklebacks (Milinski and sible (. Fig. 10.10). Firstly, females can visit Bakker 1992). The decision to stop searching a certain number of males and then select the at a certain point also depends on the prob- .. Fig. 10.9 Sampling tactics for mate choice. As with Instead, each female chooses the best male for her based these Malagasy frogs (Aglyptodactylus securifer), there on certain criteria. (Manfred Eberle) is no absolute best male that everyone should choose.
10.3 · Mechanisms of Mate Choice 213 10 .. Fig. 10.10 Tactics of mate selection. In the best-of- the sequential hierarchical reduction (bottom), pre- N tactic (above), a certain number of males are com- selections are made in stages according to different cri- pared and then the best one is chosen. If there is a teria until the right male is found. Differences in quality threshold value for the quality of the males (middle), the among males are represented by symbols of different first male that reaches this threshold value is selected. In sizes. (After Mays and Hill 2004) ability of finding a male of better quality, involve risk can also be reduced by some indi- taking into account additional costs. When viduals opting not to make their own indepen- this factor is included in theoretical models, dent choices, but rather imitating the choices the threshold tactic always proves to be more of other females. Dugatkin (1992) was the efficient on average than the est-of- tactic b N first to demonstrate such mate copying by pre- (Real 1990), because it avoids further costs if senting a female guppy with two males, one an acceptable male is found relatively early in of which was associated with the model of a the search. female. When the model was removed and the However, if the search costs are low, females female was able to move freely, she showed a should visit several males and then choose the clear preference for the male that was previ- best of this sample. When female barking tree ously associated with the model. If one first frogs (Hyla gratiosa) were simultaneously allows females to express a spontaneous pref- exposed to male calls from eight loudspeakers erence for a male, one can even reverse the placed in a semicircle, with only one of them preference of the females in a second pass having preferred characteristics, the females with this paradigm (Dugatkin and Godin would approach this one loudspeaker only 1992). These copying effects can also be dem- when it was not too far away. If all sounds onstrated in relation to the rejection of certain were played from the same distance, all of the males (Witte and Ueding 2003); females thus females would visit at least four loudspeakers; pay attention not only to who is chosen by sometimes even all eight (Murphy 2012). others but also to who is rejected. Search costs and other aspects of mate In the case of long-lived species, search choice that require time and/or energy or tactics and choice decisions could eventually
214 Chapter 10 · Intersexual Selection: How Females Choose be influenced by experience based on previ- with differences or changes in an individual’s ous decisions. Females mating for the first condition, i.e. ultimately with physiological time and those who had a male of high or low factors. For example, crickets infected with a quality in the last breeding cycle should there- parasite, compared to females in better con- fore search for different lengths of time. The dition, exhibited no preference for males with fact that females adapt their search tactics higher song rates (Beckers and Wagner 2013). based on experience has been demonstrated Female zebra finches whose physical condi- in silk bowerbirds (Ptilonorhynchus violaceus). tion was compromised by trimming their Their females visit several males one after flight feathers also associated with attrac- the other, the latter of whom wait year after tive males much less frequently afterwards year at the same bower for female visitors. (Burley and Foster 2006). Female wolf spi- Using data from simultaneous video record- ders (Schizocosa spp.) that were brought up ings at more than 30 bowers, Uy et al. (2000) in an experiment under good or bad feeding showed that females who had chosen particu- conditions behaved very similarly. Only adult larly attractive males the previous year mated female spiders in good condition showed a with them again the following year and visited preference for males that also grew up under other males less frequently than females who good conditions; females in bad condition had chosen a less attractive male the previ- were not choosy and also mated with males ous year. The latter usually did not choose in bad condition (Hebets et al. 2008). These this male again and ended up searching for a studies thus revealed that females dynamically longer period of time. Attractive males were adapt their choosiness to their assessment of defined by their independent mating success their own attractiveness. 10 with other females. Differences in choosiness are partly medi- ated by female behaviour. When males take the initiative, visit females that are ready 10.3.3 Choosiness for mating and invite them to mate, females have the option of either accepting or reject- When comparing mating behaviour among ing these solicitations. Since mating requires species, it is evident that there is great varia- physical cooperation by the females, they can- tion both in female choosiness and in their role not be forced to mate. For example, by moving in mating. Females of the Galapagos iguana away or sitting down, they can evade the mat- (A. cristatus), for example, mate only once ing attempts of certain males, thus express- per season (Trillmich 1983) and some cicadas ing a comparatively passive choice. However, only once in a lifetime (Cooley and Marshall females can actively search for mates and even 2004). Many female songbirds, in contrast, solicit matings from selected males. Such an choose a permanent partner, but occasion- active choice is particularly evident on leks ally mate with one or more additional males, and in species with territorial males. resulting in extra-pair copulations (EPCs; Kempenaers and Schlicht 2010). Both female chimpanzees and lionesses (Panthera leo) cop- 10.4 irect Benefits of Mate Choice D ulate hundreds of times per conception with practically all males in their group. Female If females have certain mating preferences, grey mouse lemurs copulate within a time the question arises as to what criteria they window of a few hours per year with any male use to differentiate among potential mates that shows interest, but aggressively resist any that meet these preferences (. Fig. 10.6). approach before or after this period (Eberle As a matter of principle, they should try to and Kappeler 2004). Adaptive causes for this choose a male with the highest possible qual- variation are discussed in 7 Sect. 10.6. ity. The quality of males can be judged by two Female choosiness also varies among criteria. Males can be distinguished either by females of the same species or within females genetic traits that contribute to higher qual- over time. This variation can be associated ity offspring (7 Sect. 10.5) or by traits that
10.4 · Direct Benefits of Mate Choice 215 10 directly influence the reproductive success of turn, allows them to lay more eggs (Muller females themselves by conveying a number of et al. 2016). In fruit flies, females adapt their possible advantages (see Box below). In both fecundity and egg size to the genotype of the cases, the prerequisite for an informed choice males (Pischedda et al. 2011). Besides clutch is the existence of phenotypic quality indica- size, females can also influence the quality tors that are accessible to the females and pro- of the eggs. For example, female birds with vide as honest information as possible about biparental juvenile care lay more eggs when the quality of a male. mating with attractive males, but lay larger eggs in species in which the females alone are responsible for the offspring (Horváthová et al. 2012). Potential direct benefits of mate choice Effects of mate choice on female fecundity 55 Increased fertility do not only depend on the intrinsic character- 55 Increased fecundity istics of males. In some insects, males make 55 Good father nuptial gifts, which are mostly consumed by 55 Access to high-quality territory females during copulation (Gwynne 2008). 55 Good sentinel The gifts can be prey, glandular secretions, 55 Good protector attachments of spermatophores or even 55 Reduced pathogen transmission parts of the male body, which have a direct or indirect influence on the reproductive suc- cess of the females due to their energy con- Through appropriate mate choice, females tent (. Fig. 10.11). The quality of the nuptial can potentially influence several factors that gift is usually positively linked to fecundity, directly affect their fitness. These effects are so females who have received a large gift lay most evident in traits that are closely related more eggs. Because of this advantage, females to reproductive success, i.e. fertility, fecundity should therefore prefer those males that offer and paternal care (Møller and Jennions 2001). the best nuptial gifts. The fertility of females, i.e. the proportion of Males also have an interest in offering a fertilised eggs or hatched young, varies, in gift of the highest possible quality, since, as fact, in numerous insects and vertebrates as a with scorpionflies (Panorpa vulgaris), mating function of interindividual variability in male duration is positively correlated with gift size traits. For example, body size, colour or song (Sauer et al. 1998). As the mating duration repertoire may be indicative of male quality, increases, more sperm are transferred, so that but arbitrary traits, such as the presence or colour of experimentally attached foot rings in birds, have also been found to correlate with different fertility rates of females. In an Aus- tralian frog (Uperoleia laevigata), for exam- ple, males that have exactly 70% of the body weight of the female in question fertilise many more eggs than males that weigh only 0.2 g more or less (Robertson 1990). Females prob- ably discriminate against both lighter males, because they do not have enough sperm, and heavier males, because they can submerge and drown the females during mating. The fecundity of a female, i.e. the current clutch or litter size, can also vary depend- .. Fig. 10.11 Male scorpionflies (Panorpa vulgaris) ing on male quality. Female moths (Lobesia present a nuptial gift in the form of a nutritious glandu- botrana) prefer “virgin” males, as they receive lar secretion to females ready for mating. (Andreas Ver- larger spermatophores from them, which, in meulen)
216 Chapter 10 · Intersexual Selection: How Females Choose the reproductive success of males with larger spined sticklebacks, differences among males nuptial gifts is ultimately higher. The evolu- in regard to care behaviour (fanning clutches tionary origin of nuptial gifts is presumably with oxygen-rich water) are correlated with to be seen in the fact that those males that the size of the pectoral fin (Künzler and randomly served a pre-existing preference Bakker 2000), so that females can discrimi- for such gifts were rewarded with differential nate against males on the basis of the size of reproductive success (Sakaluk 2000). In some this fin. In the blue grosbeak (Guiraca cae- mammals (e.g. Egyptian fruit bats, Rousettus rulea), male colouration correlates positively aegyptiacus), males who share food with with their feeding rates (7 Box 10.3). In the females also appear to have higher reproduc- sedge warbler (A. schoenobaenus), the size of tive success with these females (Harten et al. the males’ vocal repertoire is positively cor- 2019). related with their feeding rate (Buchanan and Males also vary in their contribution to Catchpole 2000); i.e. different characteristics parental care (Sect. 7 11.2). This paternal can serve as indicators of the same quality investment can take different forms. In three- trait in different species. Box 10.3 Indicators of paternal quality intensely coloured males are in better con- 55 Question: How do female blue grosbeaks dition, so colouration could be an honest (Passerina caerulea) recognise variation in indicator of quality. paternal quality among males? 55 Method: Males were caught, their blue 10 55 Background: Males differ in the intensity colouration was measured and their feed- of their blue plumage colouration. More ing behaviour was observed. 3.5 3.0 2.5 Feeding rate 2.0 1.5 1.0 0.5 0 5 10 15 20 25 30 35 Colour intensity 55 Result: The most intensely blue-oloured c this species. Females who choose to mate males were larger, had the largest territo- according to this trait can directly benefit ries with the most food and fed the young from better access to resources and higher of the first clutch more often than paler paternal investment. males. 55 Conclusion: Plumage colouration repre- (Keyser and Hill 2000; blue grosbeak: sents a reliable signal of male quality in Geoff Hill).
10.5 · Indirect Benefits of Mate Choice 217 10 Other traits that vary among males and that ate benefits from discriminating against males have direct fitness consequences for females with high parasite loads, because this reduces concern the quality of their territories, their the risk of transmitting these parasites to vigilance and protective qualities, and their themselves (e.g. sexually transmitted diseases) pathogen load. Variation in territory quality or their young. Indeed, in the majority of spe- has potential for direct benefits, in that a high- cies studied, a negative correlation between quality territory provides more food or protec- the intensity of male parasite load and their tion for the female and her offspring. Bitterling mating success was found (Able 1996). (Rhodeus sericeus) males, for example, defend access to one or more freshwater molluscs, in which the embryos of these fish develop for 3 10.5 ndirect Benefits of Mate I to 6 weeks. Females deposit their eggs in the Choice siphon of a mussel, from where they migrate to the gills. The sperm of the males are then In many cases, females only receive the sperm sucked through the mussel and fertilise the necessary to fertilise their eggs – and the genes eggs. The survival rate of the embryos depends they contain. In this case, females should both on the type of shell and on the number differentiate and select the quality of their of embryos already in it, so females should mates based on their genotype or the result- inspect shells carefully before laying eggs. ing phenotypes. Many secondary sexual traits Females actually avoid shells that already con- of males, especially conspicuous ornaments, tain embryos from other females. Females thus have been attributed a function in indicat- modify their direct fitness gains from choosing ing these quality differences. Due to the fact a male by comparing the resource they defend that females prefer mates with certain qual- (Candolin and Reynolds 2001). ity traits, a genetic association among female Females and their offspring may also preferences, male traits and the offspring fit- benefit from higher male vigilance, as this ness of certain parental combinations has may reduce their predation risk. In chickens, been established over evolutionary times. By dominant cocks are indeed more vigilant than choosing an appropriate male, females can other cocks (Pizzari 2003), which could partly thus improve their offspring’s growth rate, explain the preference of chickens for the for- fecundity, survival rate or sexual attractive- mer. In amphipods (Hyalella spp.), even the ness, which are considered to represent some probability of females falling victim to drag- of the most important indirect benefits of onfly larvae or predatory fish during mating mate choice. is influenced by the size of the chosen male For Darwin (1871), an unsolved problem (Cothran et al. 2012). of sexual selection theory was explaining the Males that buffer females from harass- existence of spectacular male ornaments. ment by other males through postcopulatory In particular, traits that make their own- mate-guarding also provide them with direct ers more conspicuous towards predators or benefits. Female mosquito fish (Gambusia hol- that compromise their chances of survival in brooki), for example, are often harassed by other ways represented a paradox, since they mating attempts and thus have significantly could not be explained by natural selection. reduced food intake rates. However, when Although Darwin came to the correct conclu- females approach a large male, this male drives sion that these ornaments serve to influence away all other smaller males, thus increas- female mate choice, he could not propose ing the efficiency of the females’ food intake a plausible mechanism for the evolution of (Pilastro et al. 2003). In this case, females these ornaments, since he could not yet know benefit directly from choosing males that are anything about their genetic basis. Today, as large as possible, since these are better pro- there are three different explanations for this tectors. Finally, females also derive immedi- link (Box).
218 Chapter 10 · Intersexual Selection: How Females Choose According to this notion, the preference of Causes of extravagant ornaments females for both a certain male trait and the 55 Fisher process ornament itself has a genetic basis (Bakker –– Ornament arbitrary and Pomiankowski 1995). In this case, there is –– Reproductive advantage through an inevitable genetic covariance between the increased attractiveness preference and the ornament, which leads to –– Ornament and preference positively the self-reinforcement of the female prefer- coupled ence, which, in turn, leads to an enlargement 55 Good genes models of the ornament. With this runaway process, –– Ornament is an indicator of quality one can explain how the evolution of orna- –– Quality is absolute ments larger than would be expected on the –– Good paternal genes increase offspring basis of natural selection occurs. fitness This process can be illustrated using a 55 Compatibility hypothetical example (. Fig. 10.12). Let us –– Complementary maternal and pater- assume that, in a population, there is variation nal genes among males in any trait that has a genetic –– Heterozygous advantage of offspring basis. In fish, some males may be slightly more conspicuously coloured than others, or in birds, males may differ in the length of their tail feathers. First of all, it must be explained Due to the Fisher process, ornaments can how a female preference gets associated with emerge and be enhanced by female mate choice such an arbitrary trait. For this purpose, it is because of a genetic correlation between a 10 preference and an arbitrary trait. It is also assumed that males with a certain expression of the trait took advantage of a pre-existing possible that males with certain ornaments sensory bias of the females. Males with a red are preferred because these are indicators of coloration could either be better detected by high genetic quality – their carriers have “good females, or females already had a preference genes”. Finally, females can also judge the for everything red because they often feed on quality of a potential mate by how compat- red food. It is therefore possible to imagine ible its genotype is with their own genotype, so that both the frequency of a male trait and that the offspring benefit from heterozygous a corresponding female preference for this advantages. trait exist in a population and follow a normal distribution (. Fig. 10.12a). If females now choose their mates in relation to this trait (e.g. 10.5.1 Sexy Sons Through tail length), the genetic basis of these two traits the Fisher Process gets coupled: The offspring of females with a preference for longer-than-average tails have A first explanation for the evolution of the both the genes for the preference and this par- ornaments that caused Darwin so many ticular tail length. However, the gene for the headaches was provided by Ronald Fisher preference is only expressed in daughters and (1930). The coevolution model named after the gene for tail length only in sons. As long him assumes that females that prefer attrac- as the frequency distribution of males and tive males derive an indirect genetic benefit females in the population with certain traits from this choice. This advantage is based on does not change, there is no selection for these the fact that the genetic basis of the attractive traits; preference and trait distributions main- ornament is passed on from the father to his tain their relative frequencies (. Fig. 10.12b). sons. This results in sons that are more attrac- However, if, for example, genetic drift tive than other males (sexy sons), and that causes the number of females with a prefer- thus produce more grand-offspring for their ence for longer (or shorter) tails to increase, mothers than the sons of other females that a self-reinforcing runaway process occurs, in do not have this preference. the course of which the preference and the