The evolution of parasite-defence grooming in ungulates

Grooming repertoires are exhibited by all terrestrial mammals, and removal of ectoparasites is an important ancestral and current function. Parasite‐defence grooming is regulated both by a central control mechanism (programmed grooming model) and by cutaneous stimulation from bites (stimulus‐driven model). To study the evolution of parasite‐defence grooming in ungulates, we compared species‐typical grooming behaviour with host morphology and habitat to test predictions of the programmed grooming model while taking into account phylogenetic relatedness. We observed grooming in 60 ungulate species at ectoparasite‐free zoological parks in which the confound of differential tick exposure was controlled for and stimulus‐driven grooming was ruled out. Concentrated‐changes tests indicated that sexually dimorphic grooming (in which breeding males groom less than females) has coevolved with sexual body size dimorphism, suggesting that intrasexual selection has favoured reduced grooming that enhances vigilance of males for oestrous females and rival males. Concentrated‐changes tests also revealed that the evolution of complex oral grooming (involving alternate use of both teeth and tongue) and adult allogrooming (whereby conspecifics oral groom body regions not accessible by self grooming) was concentrated in lineages inhabiting closed woodland or forest habitat associated with increased tick exposure, with such advanced grooming being most concentrated in Cervidae. Regression analyses of independent contrasts indicated that both host body size and habitat play a role in the evolution of species‐typical oral grooming rates, as previously reported. These results indicate that the observed grooming represents centrally driven grooming patterns favoured by natural selection in each lineage. This is the first phylogenetically controlled comparative study to report the evolution of parasite‐defence grooming behaviours in response to selection pressures predicted by the programmed grooming hypothesis. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 17–37.     

Testing the interspecific body size principle in ungulates: the smaller they come, the harder they groom

Tick removal grooming may be centrally regulated by an internal timing mechanism operating to remove ticks before they attach and engorge (programmed grooming model) and/or evoked by cutaneous stimulation from tick bites (stimulus-driven model). The programmed grooming model predicts that organismic and environmental factors that impact the cost-benefit ratio of grooming (e.g. body size and habitat) will influence the rate of tick removal grooming. The body size principle predicts that smaller-sized animals, because of their greater surface-to-mass ratio, should engage in more frequent tick removal grooming than larger-bodied animals in order to compensate for higher costs of tick infestation. The body size principle may be tested intraspecifically between young and adult animals, or interspecifically among species of contrasting body sizes. To rigorously test the interspecific body size prediction, we observed the programmed grooming (oral and scratch grooming) of 25 species (or subspecies) of bovids at a tick-free zoological park in which stimulus-driven grooming was ruled out. Multiple correlation analysis revealed highly significant negative correlations between species-typical mass and mean species grooming rates when habitat was controlled for in the model. Species-typical habitat type (classified along a gradient from most open to most closed) was positively correlated with mean oral grooming rate, indicating that species tended to groom at a higher rate in woodland and forest habitats (where typical tick density would be high) compared with more open environments. Species mass accounted for up to two-thirds of the variation in grooming rate across species, whereas habitat accounted for ca. 20% of variation in oral grooming. Similar results were obtained when the analysis was expanded to include 36 species/subspecies of six different families. The body size principle can therefore account for a large proportion of species-typical differences in programmed grooming rate among ungulates. However, to understand the tick defence adaptations of very large mammals that rarely or never engage in oral or scratch grooming (e.g. elephants, giraffes, rhinoceros), alternative tick defence strategies must be considered, such as thick skin, wallowing, rubbing and tolerance of oxpeckers and other tick-eating birds. Copyright 2000 The Association for the Study of Animal Behaviour.     

Growth of yellow-headed blackbird Xanthocephalus xanthocephalus nestlings in relation to maternal body condition, egg mass, and yolk carotenoids concentrations

Condition‐dependent resource allocation to eggs can affect offspring growth and survival, with potentially different effects on male and female offspring, particularly in sexually dimorphic species. We investigated the influence of maternal body condition (i.e., mass‐tarsus residuals) and two measures of female resource allocation (i.e., egg mass, yolk carotenoid concentrations) on nestling mass and growth rates in the polygynous and highly size dimorphic yellow‐headed blackbird Xanthocephalus xanthocephalus. Egg characteristics and carotenoid concentrations were obtained from the third‐laid egg of each clutch and were correlated with the mass and growth rates of the first two asynchronously hatched nestlings. Maternal body condition was associated with the growth of first‐hatched, but not second‐hatched nestlings. Specifically, females in better body condition produced larger and faster growing first‐hatched nestlings than females in poorer body condition. As predicted for a polygynous, size‐dimorphic species, females that fledged first‐hatched sons were in better body condition than females that fledged first‐hatched daughters. Associations between egg mass, yolk carotenoid content, and nestling growth were also specific to hatching‐order. Egg mass was positively correlated with the mass and growth rates of second‐hatched nestlings, and yolk concentrations of β‐carotene were positively correlated with second‐hatched nestling mass. Surprisingly, the relationship between yolk lutein and hatchling growth differed between the sexes. Females with high concentrations of yolk lutein produced larger and faster growing first‐hatched sons, but smaller first‐hatched daughters than females with lower lutein concentrations. Mass and growth rates did not differ between first‐ and second‐hatched nestlings of the same sex, despite asynchronous hatching in the species. Results from this study suggest that maternal body condition and the allocation of resources to eggs have carotenoid‐, sex‐, and/or hatch‐order‐specific effects on yellow‐headed blackbird nestlings.     

MATING SYSTEM AND SEXCUL DIMORPHISM IN LARGE TERRESTRIAL, MAMMALIAN HERBIVORES

Sexual dimorphism in mammals is not entirely satisfactorily explained by the models that are advanced to account for it among birds. This may be because species-specific styles of being dimorphic, and of attaining mature dimorphic state, are not clearly recognized. Mature dimorphism is a syndrome involving body size, appearance and weaponry; each facet and the whole syndrome may have functions in both fighting and signalling. The mature dimorphic stage has to be reached by growth and change from juvenile and sub-adult states. The occurrence of the separate facets of the dimorphic syndrome are reviewed in species of Bovidae, Cervidae and Macropodidae, large, diverse families of eutherian (the first two) and metatherian mammals, which have broadly similar ecological adaptations. In each family the smallest species tend to be homomorphic, with small, inconspicuous weapons. Greatest dimorphism in size is found in medium-sized bovids and cervids, and the larger macropodids (in which no species exceeds 100 kg male weight); the range of species showing greatest dimorphism in size also shows the most exaggerated weapons. Mature dimorphism is reached by different patterns of growth, which may be determinate and similar in the sexes (leading to homomorphism), determinate but differing between the sexes, or indeterminate and differing, both of which lead to heteromorphism. The syndromes of dimorphism and patterns of growth are associated and a classification of styles of dimorphism is presented. The adaptiveness of the styles is suggested in terms of what is known of the socio-ecology, in particular the male reproductive strategies, of the species. The various styles of heteromorphy appear to be associated with males' way of achieving polygyny: such as by non-resource-based territoriality, by dominance-determined access to oestrous females, or by wandering and formation of a consortship with pro-oestrous females. The relevance of the species' ecology of use of resources to these styles of dimorphism and mate-acquisition is briefly discussed.     

Development of secondary sexual characters and their relationship to ontogeny and seasonal reproductive period in Hyphessobrycon igneus (Ostariophysi: Characiformes)

Sexual dimorphism in size, anal‐fin shape and coloration of Hyphessobrycon igneus, Characidae, were examined. Males were more frequent at larger body sizes, confirming body size as a sexually dimorphic trait. Anal‐fin shape and the colour of all fins were the same for females and juveniles, differing only in adult males. Likewise, only adult males had bony hooks on fin rays; larger and more sexually mature males had the most numerous and developed hooks and hooks were most developed in degree and number during peak reproductive periods. Fin hooks regressed in number and developmental degree after the reproductive period, but restarted development with the beginning of the new reproductive period without completely disappearing. Results show that bony hooks have a development and regression cycle related to reproductive seasonality.     

Muscle‐dependent and hormone‐dependent differentiation of the vocal control premotor nucleus robustus archistriatalis and the motornucleus hypoglossus pars tracheosyringealis of the zebra finch

Sex differences in the vertebrate brain (brain sex) are thought to develop owing to the tissue specific action of gonadal hormones similar to the development of secundary sex characteristics of the body. Small sex differences in body anatomy could, however, retrogradely control the sexual differentiation of the central nervous system. This possibility has so far been verified only for motorneuron pools, since the connectivity of sex‐specific higher brain areas to the sexual dimorphic periphery is frequently not well known. Here, we tested whether somatic sex differences feed back on higher brain areas by bilateral denervation of the syringeal musculature of zebra finches before, during, and after onset of estrogen‐sensitive sexual differentiation of forebrain vocal nuclei such as RA (nucleus robustus archistriatalis). In the zebra finch, the sound‐producing musculature (the syrinx), the syrinx motornucleus hypolossus pars tracheosyringealis (nXIIts), and the RA are much larger in males compared to females. Tract tracing studies revealed that the volume and neuron size distribution of the nXIIts was sexually dimorphic in intact but not in animals denervated as juveniles. In contrast, the volume of RA and size of RA neurons of denervated animals were highly sexually dimorphic. Furthermore, estrogen masculinized the RA of denervated females. Thus, sexual differentiation of the RA but not of the nXIIts appears independent of somatic sex differences. The syrinx muscles are, however, important for the soma size of those RA neurons that project to the nXIIts. © 2000 John Wiley & Sons, Inc. J Neurobiol 42: 220–231, 2000     

Grooming in desert bighorn sheep (Ovis canadensis mexicana) and the ghost of parasites past

Ectoparasites such as ticks have a negative effect on host fitness,whereas parasite-defense grooming is effective in removing ticks.The central control (programmed grooming) model proposes thatanimals engage in preventive tick-defense grooming in responseto an internal timing mechanism, even in the absence of peripheralstimulation from parasites. This model predicts that smalleranimals will groom more frequently than larger ones becauseof the higher cost of parasitism for a small animal (body sizeprinciple). The peripheral stimulation (stimulus driven) modelpredicts no size-related differences in grooming rate in theabsence of tick bite irritation. We observed grooming behaviorin a Chihuahuan desert population of bighorn sheep (Ovis canadensismexicana), where ticks have been absent for perhaps thousandsof years. Although not exposed to ticks, bighorns self groomedby means of oral and scratch grooming, albeit at very low ratescompared to size-matched ungulates in both tick-infested andtick-free environments. Logistic regression and general linearmodels revealed both the probability that grooming was performedduring a 10-min focal sample and the rate of grooming when itoccurred was greater for younger, smaller age/sex categoriesof less body mass. Oral and scratch grooming were negativelyassociated with body mass during both years, with juveniles(X = 15 kg) grooming the most frequently and the oldest males(X = 70–85 kg) grooming the least. Assuming that programmedgrooming evolved in a tick-infested environment, the currentgrooming behavior of this population is a relict of their ancestralenvironment, an adaptation to the "ghost of parasites past."     

Sexual selection and senescence: male size-dimorphic ungulates evolved relatively smaller molars than females

As a general rule, males of sexually dimorphic ungulate species have evolved larger body size than females but shorter reproductive life spans as elements of their strategy for intrasexual competition for mating opportunities. Evolutionary theories of senescence predict that the durability of somatic structures should relate to the length of reproductive life span. This prediction has recently been tested for red deer (Cervus elaphus): molariform teeth of males are smaller and less durable than those of females, which corresponds with sex differences in reproductive life span. However, general evidence that male teeth are smaller than expected by allometric rules as a consequence of sexual selection for increasing male body mass requires an interspecific comparison between dimorphic and nondimorphic ungulates. Here we investigate the relationship between cheek-teeth size (occlusal surface area; OSA) and body mass in 123 species of extant ungulates. We found lower slopes for dimorphic species compared with nondimorphic ones and smaller OSA, relative to body mass, in males of dimorphic species compared with females of dimorphic species. Rates of evolution of OSA relative to rates of evolution of body mass were greater in females than in males and also greater in nondimorphic than in dimorphic species. Our results are consistent with the hypothesis that sexual selection in polygynous male ungulates favors body size more than tooth size, with possible consequences in male senescence via early depletion of male teeth compared to females.     

Size and sex of cricket prey predict capture by a sphecid wasp

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Rensch's rule in large herbivorous mammals derived from metabolic scaling

Rensch's rule, which states that the magnitude of sexual size dimorphism tends to increase with increasing body size, has evolved independently in three lineages of large herbivorous mammals: bovids (antelopes), cervids (deer), and macropodids (kangaroos). This pattern can be explained by a model that combines allometry, life-history theory, and energetics. The key features are that female group size increases with increasing body size and that males have evolved under sexual selection to grow large enough to control these groups of females. The model predicts relationships among body size and female group size, male and female age at first breeding, death and growth rates, and energy allocation of males to produce body mass and weapons. Model predictions are well supported by data for these megaherbivores. The model suggests hypotheses for why some other sexually dimorphic taxa, such as primates and pinnipeds (seals and sea lions), do or do not conform to Rensh's rule.     

Why are American mink sexually dimorphic? A role for niche separation

American mink are highly sexually dimorphic, with males being up to twice the size of females. Sexual dimorphism may arise for several reasons, including intra- or inter-sexual selection, inter-sexual competition, or divergent reproductive roles. Whether or not dimorphism arises from competition, a degree of niche separation is expected in dimorphic species. Sexual divergence in feeding niche has been reported for many species, including mink. This is likely to be manifested in a greater degree of dimorphism in those structures, such as teeth, that are used for the acquisition of prey. We tested the hypothesis that teeth and other trophic structures of male mink would be significantly larger than those of females, after controlling for underlying skeletal size differences. Canine and carnassial teeth, and several skull dimensions, were larger than predicted in males. There is good evidence that sexual dimorphism in mink trophic apparati is greater than predicted from allometry. We examined the development of dimorphism in various features with age and found that it was not consistent. Several trophic features were dimorphic amongst juveniles, and the degree of dimorphism remained relatively constant with age. Dimorphism in canines, and in relative body mass, was less apparent amongst juveniles and increased with increasing age. We discuss our results in the light of contemporary theories on the evolution and maintenance of sexual size dimorphism and argue that niche separation as a result of dimorphism in trophic features, while probably not the driving force behind sexual size dimorphism, may play a role in its maintenance.     

Benefits, Costs and Constraints of Anti-Parasitic Grooming in Adult and Juvenile Rodents

Grooming behaviour plays various roles in the health care, reproduction, and social life of an individual vertebrate. However, the reasons for the variability in time spent grooming amongst species, populations and individuals are not fully understood. We tested the hypothesis that the main role of grooming is ectoparasite removal and thus that time spent grooming by an animal reflects the costs of parasite infestation offset against the costs of grooming. The test was conducted on a rodent, Meriones crassus, that is parasitised by a flea, Xenopsylla conformis. We monitored behaviour of juvenile and adult rodents before and after flea infestation and quantified the probability of mortality of fleas with respect to the time spent grooming in adults compared with juvenile rodents. We predicted that: (1) increased costs of flea infestation (e.g. in parasitised as opposed to flea‐free rodents and in juveniles as opposed to adults) increases time spent grooming and (2) mortality probability per flea increases with increasing time spent grooming and is higher for fleas on juveniles than for fleas on adult rodents. We were interested to discover at the expense of which activity grooming is increased. Our findings established that the major role of grooming is in flea removal, as exposure to fleas evoked grooming activity in all rodents and grooming activity explained 57–70% of the variation in flea mortality. Furthermore, we showed that the rise in grooming activity was at the expense of resting. However, we found only partial support for the predicted increase in grooming time with increasing costs of flea infestation. Flea infestation did indeed increase the time spent grooming by rodents. Nevertheless, juvenile rodents who incur higher costs of flea infestation spent less time grooming than adults and sustained similar flea densities, suggesting that these hosts are constrained by some other factors, such as feeding time.     

Sexual dimorphism and species differences in the neurophysiology and morphology of the acoustic communication system of two neotropical hylids

We examined auditory tuning and the morphology of the anatomical structures underlying acoustic communication in female Hyla microcephala and H. ebraccata and compared our findings to data from a previous study (Wilczynski et al. 1993) in which we showed species differences in the traits that in males relate to differences in the species-typical calls. Female species differences in the best excitatory frequency (BEF) of the basilar papilla (BP) were similar to the differences seen in males, and females had a significantly lower BEF in H. ebraccata, but not H. microcephala. In both species, females had lower BP thresholds. Snout-vent length, head width, and tympanic membrane diameters were sexually dimorphic in both species and larger in females, whereas laryngeal components were sexually dimorphic and larger in males. Middle and inner ear volumes were not sexually dimorphic. Despite the significant species differences in laryngeal morphology seen in males, female larynges are not significantly different. Furthermore, the interaction of species and sex differences resulted in significantly different degrees of sex dimorphism in the species, particularly for the larynx, which is more sexually dimorphic in H. microcephala, and measures of body size, which are more dimorphic in H. ebraccata. Accepted: 6 December 1996     

浙江丽水虎纹蛙形态特征的两性异形和食性

用数显游标卡尺测量了407只2001—2003年9月下旬至10月上旬浙江丽水罚没的死亡虎纹蛙的体长等10个形态指标,结果表明:雌性成体体长(SUL)大于雄性成体,幼体形态无显著两性差异;ANCOVA去除SUL差异的影响后,雌性成体的头长和后肢长大于雄性成体,前肢长、眼径和耳径则小于雄性成体。前肢两侧对称性的偏移度成体大于幼体,雌性大于雄性;后肢两侧对称性成幼体和两性无显著差异。10个形态指标主成分分析的前三个主成分共解释64·6%的变异:第一主成分中头宽、眼径和耳径,第二主成分中后肢长,第三主成分中眼间距和鼻间距分别有较高的正负载系数。用NikonSMZ-1000解剖镜鉴别277只个体胃内容物中的食物种类,发现其秋季食物以节肢动物为主;成幼体和两性食物生态位宽度为3·42~5·25,食物生态位重叠度较高为0·93~0·98。分析表明,虎纹蛙局部形态特征的两性差异微弱,而体长两性异形差异显著;雌体具有较大的体形与食性无关,而可能与生育力选择的作用有关。     

Parental care behavior in the monogamous,sexually dimorphic Madagascar paradise flycatcher: sex differences and the effect of brood size

I studied the parental care behavior of the Madagascar paradise flycatcher Terpsiphone mutata in northwestern Madagascar. I especially focused on feeding, brooding and vigilance behaviors. Feeding rate did not differ between males and females, but females spent more time at the nest than males. Females dedicated their time to brooding, while males perched on the nest and were vigilant. Both parents changed the feeding rate in relation to brood size, so the feeding rate per nestling was not different among nests of different brood size. Duration of brooding by females increased with decreasing brood size, suggesting that the Royama effect, the pattern of lower feeding rate per nestling in larger broods, did not apply in this study. Males spent more time on vigilance than females. Anti-predator vigilance by males should be important for nestling survival given the high predation pressure typical of this population. In conclusion, males provide considerable parental care probably to minimize nestling starvation and to avoid nest predation. My results are not consistent with the general pattern of less parental effort by males in monogamous, sexually dimorphic species.     

The melanocyte-stimulating hormone receptor (MC1-R) gene as a tool in evolutionary studies of artiodactyles

The complete coding region of the melanocyte-stimulating hormone receptor (MC1-R) gene was characterized in species belonging to the two families Bovidae and Cervidae; cattle (Bos taurus), sheep (Ovis aries), goat (Capra hircus), muskox (Ovibos moschatus), roe deer (Capreolus capreolus), reindeer (Rangifer tarandus), moose (Alces alces), red deer (Cervus elaphus) and fallow deer (Dama dama). This well conserved gene is a central regulator of mammalian coat colour. Examination of the interspecies variability revealed a 5.3-6.8% divergence between the Cervidae and Bovidae families, whereas the divergence within the families were 1.0-3.1% and 1.2-4.6%, respectively. Complete identity was found when two subspecies of reindeer, Eurasian tundra reindeer (R.t. tarandus) and Svalbard reindeer (R.t. platvrhynehus), were analyzed. An rooted phylogenetic tree based on Bovidae and Cervidae MC1-R DNA sequences was in complete agreement with current taxonomy, and was supported by bootstrapping analysis. Due to different frequencies of silent vs. replacement mutations, the amino acid based phylogenetic tree contains several dissimilarities when compared to the DNA based phylogenetic tree.     

Sexual dimorphism and dental variability in platyrrhine primates

Leutenegger and Cheverud (1982, 1985) propose a hypothesis to explain why larger primates are more sexually dimorphic in body weight and canine size. Their hypothesis states that any factor selecting for an evolutionary increase in body size will produce an increase in sexual dimorphism in any character if either heritability or phenotypic variability is greater in males than in females for that character. They cite no evidence for heritability but give some data to suggest that males are, in fact, more variable than females. We test the latter proposition more fully using measurements on the dentitions of platyrrhine primates. Male and female phenotypic variances are not significantly different in most cases. Cases of greater male phenotypic variance are not limited to sexually dimorphic species. We conclude that the hypothesis of Leutenegger and Cheverud does not explain the observed patterns of dental sexual dimorphism, at least in platyrrhines.     

Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex‐specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RS^V), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.     

Muscle-dependent and hormone-dependent differentiation of the vocal control premotor nucleus robustus archistriatalis and the motornucleus hypoglossus pars tracheosyringealis of the zebra finch

Sex differences in the vertebrate brain (brain sex) are thought to develop owing to the tissue specific action of gonadal hormones similar to the development of secondary sex characteristics of the body. Small sex differences in body anatomy could, however, retrogradely control the sexual differentiation of the central nervous system. This possibility has so far been verified only for motorneuron pools, since the connectivity of sex-specific higher brain areas to the sexual dimorphic periphery is frequently not well known. Here, we tested whether somatic sex differences feed back on higher brain areas by bilateral denervation of the syringeal musculature of zebra finches before, during, and after onset of estrogen-sensitive sexual differentiation of forebrain vocal nuclei such as RA (nucleus robustus archistriatalis). In the zebra finch, the sound-producing musculature (the syrinx), the syrinx motornucleus hypoglossus pars tracheosyringealis (nXIIts), and the RA are much larger in males compared to females. Tract tracing studies revealed that the volume and neuron size distribution of the nXIIts was sexually dimorphic in intact but not in animals denervated as juveniles. In contrast, the volume of RA and size of RA neurons of denervated animals were highly sexually dimorphic. Furthermore, estrogen masculinized the RA of denervated females. Thus, sexual differentiation of the RA but not of the nXIIts appears independent of somatic sex differences. The syrinx muscles are, however, important for the soma size of those RA neurons that project to the nXIIts.     

Intraspecific Sexual Size and Shape Dimorphism in an Australian Freshwater Fish Differs with Respect to a Biogeographic Barrier and Latitude

Geographically structured variation in morphology is a common phenomenon in animals with environmental factors covarying with both latitude and biogeographic barriers having profound impacts on body size and shape. The Pacific blue-eye (Pseudomugil signifer) is a freshwater fish that lives along Australia’s east coast and occurs on either side of a terrestrial barrier, the Burdekin Gap. By quantifying the size and shape of males and females from 10 populations we found that Pacific blue-eyes are not sexually size dimorphism north of the Burdekin Gap whereas the degree of dimorphism was dependent upon latitude south of the barrier. Rensch’s rule was not supported as the degree of male-biased size dimorphism did not increase with increasing population mean body size. Body shape was related to body size and was sexually dimorphic south of the Burdekin Gap but not north of it. Our study represents a rare case of identifying how both body size and shape differ with respect to latitude and a major terrestrial biogeographic barrier and lends further support to the notion that P. signifer may comprise two species, or incipient species, that are separated by the Burdekin Gap.