Abstract

Skeletal histology supports the hypothesis that primate life histories are regulated by a neuroendocrine rhythm, the Havers-Halberg Oscillation (HHO). Interestingly, subfossil lemurs are outliers in HHO scaling relationships that have been discovered for haplorhine primates and other mammals. We present new data to determine whether these species represent the general lemur or strepsirrhine condition and to inform models about neuroendocrine-mediated life history evolution. We gathered the largest sample to date of HHO data from histological sections of primate teeth (including the subfossil lemurs) to assess the relationship of these chronobiological measures with life history-related variables including body mass, brain size, age at first female reproduction, and activity level. For anthropoids, these variables show strong correlations with HHO conforming to predictions, though body mass and endocranial volume are strongly correlated with HHO periodicity in this group. However, lemurs (possibly excepting Daubentonia) do not follow this pattern and show markedly less variability in HHO periodicity and lower correlation coefficients and slopes. Moreover, body mass is uncorrelated, and brain size and activity levels are more strongly correlated with HHO periodicity in these animals. We argue that lemurs evolved this pattern due to selection for risk-averse life histories driven by the unpredictability of the environment in Madagascar. These results reinforce the idea that HHO influences life history evolution differently in response to specific ecological selection regimes.

Highlights

  • Growth, metabolism, and reproductive physiology all have a role to play in the allocation of resources over individual lifespans, and have all been implicated in multiple explanatory models of life history evolution (e.g. [1,2,3,4,5,6])

  • We are introducing the term Retzius periodicity (RP) as a synonym and replacement for “periodicity” and “repeat interval” (RI) used by authors in prior studies (e.g., [2,3,14,15,16]) in an attempt to establish a unified terminology; we argue that the prior terms lack specificity and do not sufficiently address the oscillatory nature of Havers-Halberg Oscillation (HHO) physiology, respectively

  • The most obvious pattern is that anthropoids possess a broad range of mean RP values from 1 to 11 days, whereas strepsirrhines range only between 2 to 4 days

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Summary

Introduction

Metabolism, and reproductive physiology all have a role to play in the allocation of resources over individual lifespans, and have all been implicated in multiple explanatory models of life history evolution (e.g. [1,2,3,4,5,6]). Metabolism, and reproductive physiology all have a role to play in the allocation of resources over individual lifespans, and have all been implicated in multiple explanatory models of life history evolution While many of the effects of ecology on life history have been understood for some time, the manner in which the evolution of physiological systems is coordinated to achieve particular life history outcomes remains unclear. Bromage et al [2,3,7] used histological evidence from primate dental and osseous tissues to PLOS ONE | DOI:10.1371/journal.pone.0134210. To the Max Planck Society and the Alexander von Humboldt Foundation in respect of the Hard Tissue Research Program in Human Paleobiomics (TGB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

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