Mechanisms of heterochronic change and stasis for clutch size in swifts (Apodiformes)

Abstract

Since the mid-1800s, explanations in evolution have focused on adaptivity and natural selection, largely at the expense of factors internal to the organism. Today, the importance of internal factors is no longer in dispute. Progress continues to lag, however, on the design of a framework that would allow the integration of their action in evolution. Herein, as part of a wider effort aimed at testing the functionality of the general principle based upon the embryological concepts of induction, competence, and determination (dubbed developmental determination), I present a model for the evolution of clutch size in swifts. It is structured around the physiological mechanism controlling the trait. In indeterminate laying species, it involves an exogenous signal to the female, or induction, and the acquired ability to respond to this signal, or competence. The model explains, with the action of natural selection, how a 2-day shift in the onset of competence induces change in clutch size among species. Through the origin of induction, it predicts the evolutionary transition from indeterminate to determinate laying. Finally, in some species that are indifferent to the general increase in clutch size with latitude, it reveals how both types of developmental transformation may operate to create stasis.

Can birds count eggs in their nests?

“…Secondly, it is becoming increasingly apparent that invariance in timing of follicular disruption constitutes the standard avian mechanism. Invariance has now been substantiated by either experimental or inferential evidence for the Apodiformes (Apodidae; Haywood , ), Charadriiformes (Charadriidae, Laridae; Haywood ) and Passeriformes (Muscicapidae, Passeridae; Haywood , ). Among the remaining bird orders, intraspecific variation in clutch size also points to invariance in timing of follicular disruption as being the standard mechanism, with the exception of a handful of species at best (Haywood ).…”

“…By definition, A is the difference between the developmental maximum clutch size and the developmental minimum clutch size plus one (Haywood ). In indeterminate laying species of birds, assuming invariance in timing of follicular disruption, this parameter is obtained from the equation:where Int ( x ) denotes the greatest integer function, p is the rapid‐growth phase of yolk deposition (in days), i is the interval (in days) at which cohorts of follicles (each cohort leading ultimately to a single pre‐ovulatory follicle) are recruited into rapid growth, r max is the ratio of the maximum number of pre‐ovulatory follicles that survive follicular disruption to the overall number of follicle cohorts undergoing rapid growth and r min is ratio of the minimum number of pre‐ovulatory follicles that survive follicular disruption to the overall number of follicle cohorts undergoing rapid growth (Haywood , ,b, ). Empirical data from other species, namely Domestic Hen Gallus gallus domesticus (Gilbert et al .…”

“…Such a mechanism involves a signal that disrupts the growth of ovarian yolky follicles and, in species in which the number of pre‐ovulatory follicles that survive the event varies, intraspecific variation in clutch size is the end result (Paludan , Payne , Jones & Ward , Hamann & Cooke ). By definition, the range of clutch sizes created by the variable number of pre‐ovulatory follicles that survive follicular disruption, an event whose timing happens to be invariant within most bird species, is called the developmental range (Haywood , ,b, ). In indeterminate laying species, it is common to find that some clutch sizes lie outside the developmental range.…”

“…The reasons for this are multiple and include, for clutches smaller than the developmental range, (i) eggs that escaped detection by the observer (due, for example, to egg breakage or predation) or (ii) calcium‐deficient clutches (i.e. clutches impacted by a shortage of calcium; Haywood , Reynolds & Perrins ) and, for clutches larger than the developmental range, laying of extra eggs induced by a delay in follicular disruption (Haywood , , ). Such a delay results from a lack of tactile stimulation of the brood patch by eggs in the nest during the days leading to follicular disruption.…”