Temperature alters multimodal signaling and mating success in an ectotherm

Abstract

Temperature affects ectotherms in a variety of ways. These effects can be especially complex in sexual behaviors, as different sexes may be affected differently by temperature. We examined this in the jumping spider, Habronattus clypeatus. In this species, males court females using visual and vibratory signals. We tested whether key intersexual behaviors would change with temperature in similar, predictable ways across males and females. We first measured temperature and apparent activity of individuals across the day. We found that H. clypeatus are active across a wide range of temperatures (11-56°C) and are most active at times of day when temperature ranges from 13 to 46°C. Next, we performed mating experiments across behaviorally relevant temperatures. Females were more likely to allow males to progress to later stages of courtship and had higher mating rates at higher temperatures. Male visual and vibratory courtship behaviors generally became faster, higher-pitched, and lower in amplitude at higher temperatures. This relationship between temperature and signal aspects attained a roughly curvilinear shape, with an asymptote around 40°C. Intriguingly, mating rates in the lab were highest at temperatures potentially above those during peak spider activity in the field. Our results suggest that temperature's effects on behavior are complex and can affect males and females differently. This work emphasizes that understanding temperature effects on mating is critical to understanding sexual selection patterns particularly in species which use complex signals. Significance statementTemperature affects communication in most ectothermic species. Previous research has shown that temperature changes courter signals and chooser choice. However, this has never been investigated in species that use multimodal signals. We investigate how signals and choice change across temperatures in a desert-dwelling jumping spider. Using field temperature/activity modeling and a series of courtship experiments in the lab, we show that male signals and female choice change with temperature across biologically relevant ranges. Our results suggest that the temperatures at which mating is most likely occur at times of the day when animals are least active. These counterintuitive results highlight the importance of understanding how behavior in a controlled lab environment corresponds to natural field conditions as well as the importance of examining the effects of naturally occurring environmental variation on behavior.

Temperature‐related breakdowns in the coordination of mating in Enchenopa binotata treehoppers (Hemiptera: Membracidae)

“…Here, we found that patterns of thermal variation in courtship activity relate to overall mating rates across temperatures. However, the patterns of sex specificity in thermal sensitivity we found as well as the potential for one sex to constrain mating rates more than the other suggest that courtship activity alone may not be a consistent predictor of thermal sensitivity in mating (see also Brandt et al, 2018). Alternatively, temperature‐related breakdowns in reproduction may emerge from a combination of physiological and behavioral processes that occur throughout mating interactions.…”

“…The shape of thermal activity curves for courtship and mating behaviors may differ considerably from other traits and may be difficult to predict from thermal performance curves of physiological rates. For example, female Habronattus clypeatus jumping spiders are most likely to mate at hot temperatures, even though male courtship activity does not appear constrained at much lower temperatures in a laboratory environment and general activity is highest for both sexes at cooler temperatures in the field (Brandt et al., 2018).…”

“…Many studies that describe behavioral responses to temperature focus on performance traits like sprint speed and locomotion (Bennett, 1980, 1990; Cullum, 1998; Green & Fisher, 2004; Hertz, Huey, & Nevo, 1983; Lailvaux, Alexander, & Whiting, 2003); in contrast, the thermal sensitivity of mating‐related traits has received less attention (Andrew et al., 2013; but see Brandt, Kelley, & Elias, 2018; Rosenthal & Elias, 2019; Macchiano, Sasson, Leith, & Fowler‐Finn, 2019). Because reproductive behaviors are closely tied to Darwinian fitness, understanding how temperature affects mating‐related behaviors is central to understanding the fitness effects of thermal variation (Sinclair et al., 2012; Visser, 2008).…”

“…Many ectotherms mate within specific thermal windows because physiological constraints can limit mating‐related behavior to intermediate temperatures (Huey & Stevenson, 1979). For example, in sexually reproducing species, temperature‐related constraints on activity levels, mate localization, and copulatory behaviors could all influence the coordination of mating (Brandt et al., 2018; Candolin, 2019; Flanagan & Bevier, 2014; Macchiano et al 2019) with potentially important consequences for reproduction in a thermally variable environment.…”

“…When the thermal sensitivity of courtship activity in males and females are similar, patterns of mating across temperatures are likely to align with the activity levels of both sexes. However, sex‐specific thermal responses ( e.g., Kvarnemo, 1994; Cullum, 1998; Lailvaux et al., 2003; Darnell, Fowler, & Munguia, 2013; Condon et al., 2015; Brandt et al., 2018; Macchiano et al., 2019) stemming from differences in behavior and physiology—for example, differences in body size, metabolic costs, and extra heat produced by mating‐related activity (Beaupre & Duvall, 1998; Block, 1994; Brown & Weatherhead, 2000; Cullum, 1998; Kingsolver & Huey, 2008)—may generate mismatches in the timing of when males and females are most actively seeking or receptive to potential mates. When mismatches between male and female responses to temperature occur, the activity patterns of one sex could disproportionately constrain mating rates or the activity patterns of both sexes may interact to determine patterns of mating across temperatures.…”