Sex-biased initial eggs favours sons in the slightly size-dimorphic Scops owl (Otus scops)

Blanco, Guillermo; Dávila, José A.; Septiem, J. A. López; Rodríguez, Roberto Oropesa; Martı́nez, Rodrigo

doi:10.1111/j.1095-8312.2002.tb01709.x

Cited by 38 publications

(32 citation statements)

References 22 publications

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“…Indeed, the association between incubation onset and variable maternal allocations of resources, including in sex-specific pattern, in relation to ovulation order is frequently documented (e.g. Mead & Morton 1985;Bortolotti 1986;Blanco et al 2002;Eising et al 2003;Duckworth 2009). .…”

Section: Evidence For the Baldwin Effect's Processes (A) Environmentamentioning

confidence: 99%

Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect

Badyaev

2009

Phil. Trans. R. Soc. B

164

123

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When faced with changing environments, organisms rapidly mount physiological and behavioural responses, accommodating new environmental inputs in their functioning. The ubiquity of this process contrasts with our ignorance of its evolutionary significance: whereas within-generation accommodation of novel external inputs has clear fitness consequences, current evolutionary theory cannot easily link functional importance and inheritance of novel accommodations. One hundred and twelve years ago, J. M. Baldwin, H. F. Osborn and C. L. Morgan proposed a process (later termed the Baldwin effect) by which non-heritable developmental accommodation of novel inputs, which makes an organism fit in its current environment, can become internalized in a lineage and affect the course of evolution. The defining features of this process are initial overproduction of random (with respect to fitness) developmental variation, followed by withingeneration accommodation of a subset of this variation by developmental or functional systems ('organic selection'), ensuring the organism's fit and survival. Subsequent natural selection sorts among resultant developmental variants, which, if recurrent and consistently favoured, can be inherited when existing genetic variance includes developmental components of individual modifications or when the ability to accommodate novel inputs is itself heritable. Here, I show that this process is consistent with the origin of novel adaptations during colonization of North America by the house finch. The induction of developmental variation by novel environments of this species's expanding range was followed by homeostatic channelling, phenotypic accommodation and directional cross-generational transfer of a subset of induced developmental outcomes favoured by natural selection. These results emphasize three principal points. First, contemporary novel adaptations result mostly from reorganization of existing structures that shape newly expressed variation, giving natural selection an appearance of a creative force. Second, evolutionary innovations and maintenance of adaptations are different processes. Third, both the Baldwin and parental effects are probably a transient state in an evolutionary cycle connecting initial phenotypic retention of adaptive changes and their eventual genetic determination and, thus, the origin of adaptation and evolutionary change.

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Section: Evidence For the Baldwin Effect's Processes (A) Environmentamentioning

confidence: 99%

Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect

Badyaev

2009

Phil. Trans. R. Soc. B

164

123

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“…Alternatively, exposure of ovarian oocytes to specific concentrations of PRL and steroids and the corresponding accumulation of steroids in growing oocytes (Schwabl 1996) prior to meiosis might bias sex determination in birds in which the female is the heterogametic sex. Both strategies would result in often documented, but unexplained, bias in ovulation order of male and female eggs within a clutch (Ankney 1982;Dijkstra et al 1990;Krackow 1995a;Cordero et al 2001;Legge et al 2001;Blanco et al 2002;Komdeur & Pen 2002;.…”

Section: Introductionmentioning

confidence: 99%

Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird

et al. 2005

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Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.

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“…This suggestion is corroborated by the observations of precise sex bias in relation to ovulation sequence and oocyte growth patterns in birds (Blanco et al 2002;Velando et al 2002;Andersson et al 2003;Young & Badyaev 2004;Badyaev et al 2005Badyaev et al , 2006aPike 2005), patterns that are difficult to explain by mechanisms other than epigenetic effects on sex chromosome drive. Furthermore, chromosomal interactions during meiosis in heterogametic avian females should facilitate rapid evolution of mechanisms that enhance the probability of chromosome transmission to the oocyte (Zwick et al 1999;Padro-Manuel de Villena & Sapienza 2001a;Fishman & Willis 2005;Dawe & Henikoff 2006), and such mechanisms might be co-opted for sex ratio adjustment.…”

Section: Meiotic Drive and Adaptive Sex Ratio Adjustmentmentioning

confidence: 56%

Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds

Rutkowska

Badyaev

2007

Phil. Trans. R. Soc. B

144

108

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Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species.

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Sex-biased initial eggs favours sons in the slightly size-dimorphic Scops owl (Otus scops)

Cited by 38 publications

References 22 publications

Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect

Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect

Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird

Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds

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